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Article

Plant and Soil Effects of Alternative Sources of Phosphorus over Three Years of Application

by
Anna Karpinska
1,
Thomais Kakouli-Duarte
1,*,
S.M. Ashekuzzaman
2,
John Byrne
1,
Achim Schmalenberger
3 and
Patrick J. Forrestal
4,*
1
enviroCORE, Department of Applied Sciences, South East Technological University, Carlow Campus, R93 V960 Carlow, Ireland
2
Department of Civil, Structural and Environmental Engineering, Munster Technological University, T12 P928 Cork, Ireland
3
Department of Biological Sciences, University of Limerick, V94 T9PX Limerick, Ireland
4
Teagasc, Environment, Soils and Land Use Research Department, Johnstown Castle, Y35 TC97 Wexford, Ireland
*
Authors to whom correspondence should be addressed.
Agronomy 2024, 14(7), 1591; https://doi.org/10.3390/agronomy14071591
Submission received: 16 June 2024 / Revised: 18 July 2024 / Accepted: 19 July 2024 / Published: 22 July 2024
Browse Figures
Versions Notes

Abstract

:
Plant growth and food security depend heavily on phosphorus (P). Recovering and recycling P from animal, municipal, and food waste streams can significantly reduce dependency on traditional mineral P. This is particularly pertinent in the EU regions with limited native P supplies. The agronomic performance of including P-based recycling-derived fertilisers (two struvite and two ashes) or cattle slurry was compared to a conventional mineral P fertilisation programme along with no P and no fertiliser controls over three years. A field-scale experiment was set up to evaluate the perennial ryegrass dry matter yield (DMY), P uptake, and soil test P effects. Struvite, ash, and cattle slurry proved effective in replacing P mineral fertiliser and produced yields similar to those of the mineral fertiliser programme. Differences were observed in plant P recovery, with struvite-based programmes achieving a significantly higher P recovery than ash-based programmes, which had the lowest plant P recovery. Differences in Morgan’s soil test P were also noted, with potato waste struvite (PWS) and poultry litter ash (PLA) showing significantly higher soil test P values. The findings strongly indicate that a range of recycled bio-based fertilisers from the bioeconomy can be used to reduce reliance on conventional imported mineral P fertiliser, with some programmes based on recycled fertilisers even surpassing the performance of conventional linear economy mineral fertilisers.

1. Introduction

Phosphorus (P) is an essential nutrient supporting physiological and biochemical processes in plants, including cell division and cell growth, energy storage and transfer, respiration, and photosynthesis [1]. Phosphorus deficiency in soil reduces overall plant growth, root development, and yield in grasslands [2,3,4] and agricultural systems [5]. Rock phosphate, a primary P source, is geographically concentrated within five countries (Morocco, China, Algeria, Brazil and Syria), controlling 85–90% of the world’s active reserves [6]. Furthermore, the supply of rock phosphate in the Northwestern Region of Europe (NWE) is insufficient for current P demands [7]. Rock phosphate is manufactured into different types of P fertilisers. Common mineral phosphorus-based fertilisers are single superphosphate (SSP) and triple superphosphate (TSP). A chemical reaction between phosphate rock and sulphuric acid produces SSP, while TSP is generated by the chemical reaction between phosphate rock and phosphoric acid [8]. Some P reserves are only suitable for use with prior treatment [9] due to contaminants like cadmium (Cd) in rock phosphate [10]. In 2019, the European Union (EU) introduced new limit values for pollutants in different fertiliser categories to reduce health and environmental risks and to guarantee soil protection [11]. The EU is particularly concerned about the Cd content in mineral fertilisers, as it is a toxic heavy metal ranked as a class 1 carcinogen by the World Health Organization [12]. Cadmium can bioaccumulate in soils and be absorbed by crops, increasing contaminant levels in the food chain [13,14].
Due to the depletion of world P resources and the adoption of sustainable food production approaches, it is sensible to increase the recycling of P from urban and agricultural wastes [15,16,17,18]. The circular economy aims to integrate nutrient recovery technologies (NRTs) or bio-based technologies (BBTs) to make economically viable products using waste as input [19,20]. Recycling-derived fertilisers (RDFs) or bio-based fertilisers (BBFs) are products made from organic waste materials, including animal manure, sewage sludge, food processing and municipal solid waste. Valuable nutrients are recycled back into agricultural fields by generating and applying RDFs, thus developing the circular economy [21,22]. The utilisation of BBTs and recycling wastes into the production of RDFs presents an opportunity for increased sustainability of agricultural practices and the development of a circular nutrient economy. Grasslands in Ireland produce some of the highest grass yields in Europe [23] and contribute to milk and meat production globally by providing part of the feed for ruminants [24]. In Ireland, grass is the most affordable feed source of nutrients for grazing animals, and grassland ecosystems serve as the foundation for sustainable livestock production [25]. However, within the NWE territory, Ireland was identified as a region with a shortage of P and the potential region to replace mineral P fertiliser with the RDFs [26].
Crystallisation and precipitation technologies can produce ammonium magnesium phosphate mineral (MgNH4PO4.6H20) called struvite [27,28], while the use of incineration technologies with P-containing feedstocks can result in the production of ashes [29,30]. The objective of the present field study was to (1) perform an agronomic and soil fertility assessment of four RDFs (two struvites and two ashes) where they are used to displace mineral fertiliser reliance in a fertiliser programme in grassland, (2) evaluate their performance as sustainable substitutes for mineral P fertiliser, and to (3) establish their field performance when integrated into a fertiliser programme. In the work presented here, we hypothesised that the RDFs have the potential to serve as a valid source of P and a sustainable alternative to conventional mineral fertilisers. The perennial ryegrass dry matter yield (DMY), P uptake by grass, soil available P and the chemical composition of RDFs are presented. The field study findings provided valuable insight into plant and soil response to different RDFs. Furthermore, the agronomic performance of novel RDFs was assessed to facilitate their use as innovative solutions for sustainable agriculture and the circular economy.

2. Materials and Methods

2.1. Experimental Set-Up and Design

The field experiment was performed at the Teagasc, Johnstown Castle, Environment, Soils and Land Use Research Centre, County Wexford, Ireland (Figure 1), as part of the Interreg NWE ReNu2Farm project. The goal of ReNu2Farm was to increase the production and use of recycled plant nutrients in the primary food production chain in NWE. A three-year field study was conducted on a P-deficient site, with an average soil Morgan’s P level of 2.9 mg L−1 at the beginning of the trial. As per the Irish classification system [31], Morgan’s soil test Pvalue corresponds to the lowest soil P Index of 1, where the P response is expected to be definite [31]. The soil texture was a sandy loam, and the initial average pH of the soil was 5.6. Lime was applied at a rate of 1.5 (t ha−1) at the start of the experiment in accordance with agronomic recommendations. Perennial ryegrass [vars. AberGreen (40%), AberChoice (30%), and AberGain (30%), Germinal Ireland Ltd. (Thurles, County Tipperary, Ireland)] was sown in September 2018, and initial fertiliser application occurred seven months later, in April 2019.
A randomised block experiment with five replicates per treatment was conducted, with each treatment plot being 2 m × 6 m in size. Negative controls included a no-fertiliser treatment (NF) and a no-phosphate treatment (SP 0). Furthermore, two commonly practised conventional P fertiliser treatments were used: (1) superphosphate (SP) based 100% on mineral P and (2) cattle slurry (CS) with a combination of mineral P. Superphosphate is a 16% P TSP-based fertiliser P source, with the source of P being TSP. The RDF treatments included two struvites, one derived from potato processing waste (PWS) and the other from municipal waste (MWS), and two ashes, one derived from poultry litter (PLA) and the other from sewage sludge (SSA). The P requirements of the RDF fertiliser programmes were supplied in full by the RDFs.
The design of this field trial was such that each treatment was balanced in required macronutrients, such as N (nitrogen), P, K (potassium), and S (sulphur), using mineral fertiliser to meet crop nutrient requirements as the RDFs and the cattle slurry did not supply the balance of nutrients required. Depending on the source, RDF can contain different amounts of nutrients and have different chemical compositions (Table 1). Where RDF also contained N, K, or S, these nutrients were considered, and only enough chemical fertiliser was supplied to meet the recommended dosage to achieve balanced crop nutrition. Nitrogen was provided through calcium ammonium nitrate (CAN; 27% nitrogen). Potassium was delivered in the form of muriate of potash (MOP; 50% K) and sulphate of potash (SOP; 42%K and 18% S). Sulphur was supplied during the SOP application. This trial also served as a demonstration trial for farmers to see the effects of displacing mineral fertilisers in a programme. The SP 0 treatment received no P (mineral NKS only). The SP treatment received P, N, K, and S in the mineral form and was the reference treatment for a mineral-fertiliser-only programme.
In 2019, 2020 and 2021, the first application of nutrients took place in April. The second application occurred in May and the third one in July. There were a total of nine nutrient applications over three years corresponding to a three-cut silage system. During the first application, the N, K, and S fertilisers were applied in the mineral form at the recommended dosages of 125 kg N ha−1, 155 kg K ha−1, and 20 kg S ha−1. Phosphorus was applied at a rate of 40 kg P ha−1 in the form of conventional fertilisers (positive control) or the RDF treatments under test. Control treatments received no P and no fertiliser in the case of the no fertiliser (NF) control. During the second and third applications, the N, K, and S as mineral fertilisers were applied at dosages of 100 kg N ha−1, 75 kg K ha−1, 20 kg S ha−1, and P was applied at 10 kg P ha−1. In 2021, the P fertiliser in the form of chemical fertilisers or RDF was applied at the rate of 20 kg P ha−1 for the first harvest due to increased soil test P following the previous years. All other nutrient rates and timings were as in 2019 and 2020. Due to supply issues, the MWS treatment was discontinued in the final year of the trial (i.e., 2021).

2.2. Harvests, Crop and Soil Analysis

A total of nine grass harvests were conducted between 2019 and 2021 (24 May 2019, 17 July 2019, 26 September 2019, 14 May 2020, 7 July 2020, 18 August 2020, 11 June 2021, 29 July 2021, and 23 September 2021). Plots were harvested using a Haldrup (DEUTZ-FAHR, Lauingen, Bavaria, Germany) grass harvester. A detailed harvest technique, standard sample preparation and analytical techniques used to determine the soil and grass parameters can be found in Ashekuzzaman et al. (2021) [32]. For instance, fresh grass subsamples were weighed and then dried in perforated plastic bags in an oven at 70 °C for 72 h for the dry matter analysis. After drying, the samples were ground and sieved to a 2 mm size prior to use for nutrient analysis. The crop P content was analysed using an Agilent 5100 ICP-OES (AGILENT TECHNOLOGIES) synchronous vertical dual view inductively coupled plasma optical emission spectrometer, following the microwave-assisted acid digestion of dried and sieved grass samples [33]. Fresh soil samples were taken in a “W” shaped pattern to a depth of 10 cm per plot. Samples were dried at 40 °C for 72 h and then mechanically ground to a size of <2 mm. Morgan’s reagent solution [34] as used to determine extractable soil P, followed by the calorimetrical analysis conducted on the Lachat QuickChem 8500 Series 2 (HACH) continuous flow analyser. Soil pH was determined using a pH electrode (METTLER-TOLEDO).

2.3. Chemical Characteristics of Mineral and Bio-Based Fertilisers

The RDFs and CS were analysed to determine their nutrient, metal and total carbon (TC) contents using the methodology presented by Shi et al. (2022) [35]. Briefly, nutrients and metals were examined by an Agilent 5100 synchronous vertical dual view inductively coupled plasma optical emission spectrometer (Agilent 5100 ICP-OES) following the microwave-assisted acid digestion of the fertiliser samples. The TruSpec CN analyser (LECO) was employed to determine TC and total nitrogen (TN) using a high-temperature combustion method. The superphosphate mineral P fertiliser sample (200 g) was analysed by ALS Life Sciences Ltd. (Na Harfe 336/9, Prague, Czech Republic) for chemical analysis. The macro- and microelements were determined by atomic emission spectrometry with inductively coupled plasma [36]. The TN was determined by a modified Kjeldahl method and spectrophotometry [37]. The sample was homogenised and mineralised with aqua regia prior to metal analysis. Before TC analysis, the P mineral sample was dried at 105 °C and pulverised.

2.4. Statistics

Using quantitative soil and grass data collected by Teagasc between 2019 and 2021, statistical analyses were conducted in IBM SPSS Statistics for Windows, version 28 [38]. The differences among the treatments were tested for significance (p ≤ 0.05) using the one-way ANOVA test with the Bonferroni Post Hoc test for multiple comparisons. The Benjamini–Hochberg correction test was utilised to correct for multiple comparisons and decrease the number of false positive significant results [39].

3. Results

3.1. Nutrient and Metal Characteristics

According to the new EU Fertiliser Products Regulation [11], a solid organic fertiliser shall contain at least one of the primary nutrients such as N, P or K and Org C (organic carbon) of solely biological origin. Furthermore, where the solid organic fertiliser contains more than one primary nutrient, the total N (Norg, NH4+, and NO3–) content should be equivalent to a minimum of 1%, the P content should be a minimum of 1% as phosphorus pentoxide (P2O5), or K should be equivalent to a minimum of 1% as potassium oxide (K2O). Org C content in the solid organic fertiliser shall be at least 15% by mass. The conversion factor 0.436 can be applied to express P2O5 as P and a factor of 0.830 to express K2O as K [11]. Recycling-derived fertilisers in this study contained more than one primary nutrient (Table 1). Both struvites fulfilled the N content requirements, but the concentration in both ashes was not at the minimum required level. All RDFs had a P content above the minimum, but the P concentration in the PWS (106.7 g kg−1) and MWS (100.3 g kg−1) was almost twice as high as that in the PLA (55.1 g kg−1) RDF. The MWS contained less K than the minimum, but the PLA was found to have the highest K concentration of 106.7 g kg−1. All RDFs have met the minimum requirement of at least one primary nutrient (N, P, or K) being above the level specified in the EU fertiliser regulation. However, the TC content of both struvites and ashes was below the threshold of 15% by mass. The EU Fertiliser Products Regulation [11] also introduced new limit values for contaminants, such as heavy metals (i.e., Cd, Hg, As, Ni, Pb, Cr {VI}, Cu, and Zn) in different fertiliser categories. The heavy metal profile of ashes differed from that of struvite (Table 1). The concentration of Cu and Zn in the ash products under this study (PLA and SSA) exceeded the maximum EU-allowed concentration in the organic fertiliser; however, neither ash nor struvite meets the TC threshold required to be considered organic fertilisers. In the case of ash, a large concentration effect occurs during the combustion of TC and other elements compared to raw manure. Using the organic fertiliser framework, despite the observation noted, the Ni concentration of 58.7 mg kg−1 for SSA does not exceed the mineral fertiliser limit of 100 mg kg−1. The mineral fertiliser Ni concentration was 29.4 mg kg−1 compared with 21.8 mg kg−1 for PLA and 58.4 mg kg−1 for SSA (Table 1). No exceedances of any heavy metal content occurred for either struvite. The cadmium level of 17.8 mg kg−1 in the conventional mineral P fertiliser (SP) was high compared to all four RDFs, which ranged from <0.15 to 1 mg kg−1. However, the maximum level for inorganic fertiliser allowed by the EU of 60 mg kg−1 was not exceeded. The CS has met the necessary requirements for all primary nutrients and Org C content, and the contaminant levels did not exceed the maximum allowed concentration in the organic fertiliser, as per EU guidelines. Although the P content in the CS treatment was low compared to other fertilisers, the N content was higher than that in both ashes, and the K and S content was higher than that in both struvites (Table 1).

3.2. Grass Annual Yield and P Uptake by the Grass

3.2.1. Grass Yield

The average annual grass dry matter yield (DMY) associated with the experimental treatments and controls is presented in Figure 2. Over three years (2019, 2020, and 2021), the unfertilised control (NF) produced significantly lower DMY (p = 0.001) when compared with the fertilised treatments (i.e., all other treatments). Although the grass DMY (kg ha−1) between the SP 0 treatment (NKS only) and the SP mineral fertiliser treatment (NPKS) did not differ significantly, the trend from the P addition was for increases in the average total grass DMY by 919.0 (kg ha−1) in 2019, 1032.0 (kg ha−1) in 2020, and 1108.0 (kg ha−1) in 2021. Furthermore, in 2020, the grass DMY observed in the PWS, MWS, and SSA RDFs increased (+721 kg ha−1, +523 kg ha−1, and 301 kg ha−1, respectively) compared to the SP mineral fertiliser treatment.

3.2.2. P Uptake

The average annual P uptake of experimental treatments and controls is shown in Figure 3. Over three years, the NF treatments produced significantly lower (p < 0.05) P uptake (ranging from 11.4 to 14.5 kg P ha−1) compared to the SP 0 treatments (24 to 27.5 kg P ha−1) and the other remaining treatments (ranging from 24.5 to 42.8 kg P ha−1). In 2019, the SP 0 treatment showed significantly lower (p < 0.05) P uptake than in all treatments receiving P, apart from the PLA and SSA treatments, which were not significantly different. In 2020, the SP 0 treatment showed significantly lower (p < 0.05) P uptake than in all other treatments receiving P, apart from the PLA treatment. In 2021, the SP 0 treatment had significantly lower P uptake (p < 0.05) than all other treatments receiving P apart from the PLA and CS. The PWS treatment gave significantly higher P uptake (p < 0.05) compared with both ashes (PLA and SSA) in 2020 and 2021 and all other treatments in the final year of the trial. The MWS treatment showed significantly higher P uptake (p < 0.05) in 2019 and 2020 compared with the PLA treatment. In 2020, P uptake was significantly higher (p < 0.05) for the SP mineral treatment than the PLA treatment, although it was not in 2019 or 2021.

3.3. Soil P

The pre- (April 2019) and post-harvest (September 2019, October 2020, and October 2021) average soil P concentrations (Morgan’s P mg L−1) are shown in Figure 4. The beginning soil P test shows no significant difference (p = 0.526) between the treatments, as would be the goal before treatment application. In the end-of-season soil analysis from 2019, the PWS and PLA treatments had significantly higher Morgan’s P (p < 0.05) than the CS, SSA and SP mineral treatments, whereas, in the end-of-season analysis from 2021, only the PWS treatment had significantly higher Morgan’s P (p < 0.05) than the CS, SSA and SP mineral treatments. In the end-of-season soil analysis from 2020, the PWS and PLA treatments had significantly higher Morgan’s P (p < 0.05) than the SSA and SP mineral treatments. Over three years, the PWS and PLA treatments were observed to have significantly higher Morgan’s soil P concentrations than the NF and SP 0 treatments. The MWS treatment had a significantly higher soil P when compared with that observed in the NF, SP 0, CS and SP treatments in 2019. Soil test P for the CS and the SP treatment did not differ during this three-year study. At the end of the last year of the trial (Figure 4), the PWS treatment was found to have the highest soil P concentration, followed by the PLA RDF. Both treatments reached a soil P index of 4 [31] after beginning at index 1. Thus, these two treatments appear to have the strongest effect in building soil test P.

4. Discussion

Phosphorus is essential for several physiological and biochemical processes in plants, such as photosynthesis, respiration, energy storage and transfer, cell division, and cell enlargement [1]. Water, solar radiation, and nutrients are the most important factors promoting plant productivity [40]. In the present study, the unfertilised control (NF) gave significantly lower DMY (Figure 2) and P uptake (Figure 3) than was observed in the other treatments. The SP 0 treatment received N, K, and S, but no P. Although the grass DMY between the SP 0 treatment (NKS only) and the SP mineral fertiliser treatment (NPKS) did not differ significantly, the addition of mineral P in the SP treatment increased the average grass DMY by a total of 3059.0 (kg ha−1) over three years or by 1020.0 kg DMY/year on average. Furthermore, the DMY tended to increase when using both struvites (PWS and MWS); however, yields were not significantly different from those of the remaining P treatments. Neither were significant differences observed for DMYs when using ash products or when using cattle slurry compared to the mineral fertiliser P programme. These results indicate that similar yields can be achieved when conventional mineral P fertiliser is substituted by the struvite, ash, and cattle slurry tested over a three-year application programme. In the O’Donnell et al. (2022) [41] study, low solubility struvite increases the soil P levels while producing a sustainable DMY and sheds light on the benefits of recovered struvite fertiliser as a sustainable and renewable P source.
Notably, the P uptake by grass (Figure 3) was significantly increased when using struvites. In contrast, it significantly decreased with the use of ashes, indicating a P availability difference between the two types of RDF even though no DMY difference was detected. The struvite-based fertiliser programme showed greater P uptake in the grass than the ash-based programme, indicating greater plant availability for struvites than the ashes tested. This lower uptake may be due to either a low availability of P for plant uptake associated with the ash products, the presence of P-sorbing metals (Al, Fe, and Ca) in the ash products, or both factors. The crop available fraction of P in ashes can vary across different bio-based products [42]. According to Ohno and Erich (1990) [43], plants could only utilise a small amount of the P recycled in the form of wood ash. Poor solubility of P in biomass ashes was also described by Pels et al. (2005) [44]. In contrast, in a study by Li et al. (2016) [45], biomass ashes had P availability similar to that of mineral phosphate fertiliser. In a study by Talboys et al. (2016) [46], P fertiliser in the form of struvite was reported to have low water solubility and slow-release fertiliser, unlike commercial fertiliser.
In Ireland, Morgan’s extraction method has been adopted [31] to indicate plant-available P (mg L−1) in soil. Morgan’s P test is currently the standard soil test used by state bodies (e.g., Teagasc, EPA) and the agricultural sector in Ireland. Using the available soil P test, the soil index system categorises soils into one of four soil P indexes. Grasslands with soil indexes of 1 (0–3 mg L−1 Morgan’s P) and 2 (3.1–5 mg L−1 Morgan’s P) have higher P requirements relative to high index levels, and the soil P reserves may be insufficient to meet crop demand [31]. Soils with a P index of 3 are considered the most suitable for agronomical production and meeting the high yield requirements of the crop. Index 4 indicates that soil P reserves are adequate to meet crop demands for the growing season without the addition of P fertilisers in most cases. The soil P index for the PWS and PLA treatments reached index 4 for grassland (above 8 mg L−1 Morgan’s P) at the end of the growing season in 2021. In contrast, the remaining fertiliser P-containing programmes reached a soil P index of 3 (5.1–8 mg L−1 Morgan’s P). Furthermore, over three years, the PWS and PLA treatments were observed to have a significantly higher Morgan’s P when compared with various P treatments (i.e., NF, SP 0, CS, SP, and SSA); thus, these two treatments appear to have the strongest effect in building soil P test. Although the PWS and PLA fertiliser programmes both reached a soil P index of 4, the P uptake observed in the PWS treatment was significantly higher than in the PLA treatment. These results indicate a superior soil P availability over the longer term where struvite is used to deliver P in a fertiliser programme compared to the other sources of P tested.
Furthermore, Khiari et al. (2020) [47] reported a link between the amount of Al and Fe in wastewater-treated sludge and reduced P availability to plants. A high content of P-sorbing metals (Al, Fe, and Ca) is one of the factors affecting the efficiency of recycled P as a fertiliser [48,49]. Iron and Ca are known to affect soil P availability negatively [32]. The amount of Ca content exceeding a molar Ca:P ratio of two in organic fertilisers can negatively affect the P availability for plant uptake [50,51]. In contrast, Hylander and Simán (2001) [52] found that the P bound to Ca is more available to plants than that bound to Al and Fe. The composition analysis of the PLA and SSA products showed the presence of Al, Fe, and Ca (Table 1). The Fe and Al content (59,622.1 mg kg−1 and 52,979.9 mg kg−1, respectively) in the SSA treatment were relatively high compared to the amounts of Fe and Al (4632.7 mg kg−1 and 7459.5 mg kg−1, respectively) in the PLA product or in the SP (914 mg kg−1 and 1900.0 mg kg−1; Table 1). Additionally, a molar Ca:P ratio associated with the PLA was higher than that in the SSA (3:1 and 1:1, respectively). Although the PLA delivered high levels of soil available P (Figure 4), at the same time, it gave the lowest P uptake by grass compared with the remaining P treatments and significantly lower compared with both struvites. The PLA was the only treatment in which the molar ratio of Ca:P was 3:1. In the study by Ashekuzzaman and colleagues [32], the Al concentration in aluminium dairy processing sludge did not limit P bioavailability. Instead, low P bioavailability, recorded for the calcium dairy processing sludge, was associated with high Ca content, the formation of low soluble Ca-P compounds, and a high Ca:P ratio. Notably, the amounts of Fe, Al, and Ca in struvites were very low.
Barrow and Hartemink (2023) [53] recently reported that soil pH can affect P availability and plant P uptake rate. The optimum soil pH for grassland is at or above 6.3. Therefore, Teagasc (2020) [31] sets the target pH at 6.5. According to Teagasc (2015) [54], a pH between 5.8 and 6.8 is suitable for P to be available for plant uptake. Fixation of P by Al and Fe can occur in acidic soils, whereas in alkaline soils, P can be fixed by Ca [54]. The soil pH was maintained between 5.8 and 6.5 throughout the field experiment. Additionally, no statistical difference in soil pH among the treatments was recorded over the course of the study.
Phosphorus mineral fertilisers, such as triple superphosphate (TSP), are used in Ireland’s agricultural sector to promote plant growth [31]. These P fertilisers are manufactured using phosphate rock as a base material. Phosphate rock contains cadmium (Cd), and the concentration of the heavy metal may vary between 1 to 150 mg kg−1 [9,13], depending on the rock phosphate type (i.e., sedimentary, volcanic, or igneous). Cadmium can accumulate in soils and be absorbed by crops, increasing the contaminant levels in the food chain [13,14,55]. The World Health Organization classified Cd as a class 1 human carcinogen [12] that bioaccumulates with age in the kidney or liver [56]. In addition to smoking, humans are exposed to Cd primarily through their diet [57]. The new EU Fertiliser Products Regulation [11] introduced new limit values for contaminants in different fertiliser categories to reduce health and environmental risks and guarantee soil protection. The maximum allowed Cd concentration threshold in inorganic fertilisers is 60 mg kg−1; in organic fertilisers, the upper limit is 1.5 mg kg−1 [11]. According to a recent study by Ballabio et al. (2024) [58], Irish topsoil has been identified as containing the highest average Cd concentrations (>1 mg kg−1) compared to other European soils. The concentrations of Cd (Table 1) in the inorganic fertiliser (SP), CS, and RDFs under this study did not exceed the maximum Cd levels allowed by EU regulation. Although the Cd concentration in the mineral fertiliser (17.8 mg kg−1) was within the legal limits, P fertilisers, such as the RDFs, all contained much lower levels of Cd (<1 mg kg−1) and, therefore, are also desirable products that can minimise the potential for Cd accumulation in soil and minimise human exposure in a long-term scenario.
Bio-based fertilisers such as struvite and ash products have been evaluated in multiple studies [59,60,61,62,63,64,65,66,67,68,69]. In the ecological studies by Karpinska et al. (2021) [65] and Ryan et al. (2022) [66], soil bacterial, fungal, and nematode communities of the struvite treatments (i.e., PWS and MWS) were similar to those in the P mineral treatment. Communities in the ash treatments (i.e., PLA and SSA) were more disturbed in their compositions and abundances, possibly due to relatively higher concentrations of certain heavy metals [65,66]. A short-term pot trial was conducted by Deinert et al. (2023) [67] to study the impact of the same RDFs tested in the current field trial (MWS, SSA, and PLA) on the perennial ryegrass growth and the soil P-cycling microbiota. According to Deinert et al. (2023) [67], struvite application increased plant dry weights, and available P acid phosphatase activity was significantly improved at the high P application rate (60 kg P ha−1). Meanwhile, the PLA RDF negatively affected acid phosphatase activity at the high P application rate. In contrast, in a study by Deinert et al. (2024) [69], the struvites (i.e., PWS and MWS) either positively influenced the P cycling microbial community or did not affect it. In general, struvites are reported as slow-releasing P fertilisers [45] that can provide a long-term P source for crop growth and meet the plant’s demand for P during the late stages of the growing season [70]. On the other hand, ash products generally tend to have poorer availability of P compared to struvite and, in some cases, higher content of certain metals [32,34,61]. Ash producers are developing new methods to reduce the heavy metal load in their final products and, at the same time, improve the availability of P when in soil [71].
With respect to the new EU limits for heavy metals in fertilisers [11] and a relatively high Cd concentration in certain Irish topsoils that has been reported [58], the use of bio-based struvites, low in heavy metal content, should be recommended as a recycled P alternative to the mineral forms with higher Cd content, where possible. The heavy metals (i.e., Cd, Hg, As, Ni, Pb, Cr [VI], Cu, and Zn) in the PWS and MWS RDFs used in this study were well below the EU-regulated limits. Both struvites (i.e., PWS and MWS) were produced with Nutrients Recovery Systems (NuReSys®) technology [72]. In the current study, the displacement of mineral P fertiliser with cattle slurry, struvites or ash resulted in similar yields, demonstrating the potential for using recycled sources of P and other nutrients to lessen reliance on mineral fertiliser. Further research is warranted to understand the plant availability and soil fertility effects of potential P-sorbing metals in the final ash products.

5. Conclusions

Struvites were found to be a promising source of recycled P and a sustainable alternative to the P mineral fertiliser. This is due to (1) good grass yield and P uptake by grass, (2) a high plant availability of soil P over the three-year study, and (3) very low levels of environmental contaminants such as heavy metals, including Cd. While the fertiliser programmes using ash produced similar DMY to the other programmes, there was a trend for lower plant P recovery compared to struvite. For certain heavy metals, specifically Zn, Cu, and Ni, levels were higher than those of other products tested, some of which exceeded the EU-regulated limits of organic fertilisers. However, the ash materials tested do not contain enough TC to be considered organic fertilisers. Using the mineral fertiliser limits as a reference point (1500 mg kg−1 for Zn, 600 mg kg−1 for Cu, and 100 mg kg−1 for Ni), limits were not exceeded for the ash products tested.
Policymakers should be aware that not all RDFs are the same in terms of composition and field performance. Nevertheless, these products have an important role to play in developing the local bioeconomy and lessening conventional imported mineral fertiliser reliance in Europe and other regions. This study demonstrates the importance of field-testing RDFs. Struvites have a considerable and very promising potential to replace traditional chemical fertilisers. Therefore, there is a continuous need for research and innovation in producing RDFs. Production processes for all fertilisers should be optimised to minimise the heavy metal content.

Author Contributions

Conceptualisation, A.K. and P.J.F.; methodology, A.K., S.M.A., P.J.F. and J.B.; software, A.K.; formal analysis, A.K.; investigation, A.K., P.J.F. and J.B.; resources, T.K.-D., A.S. and P.J.F.; data curation, S.M.A. and P.J.F.; writing—original draft preparation, A.K.; writing—review and editing, T.K.-D., J.B., S.M.A., A.S. and P.J.F.; visualisation, A.K., J.B. and P.J.F.; supervision, T.K.-D. and J.B.; funding acquisition, T.K.-D., A.S. and P.J.F. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Interreg Northwest Europe project “ReNu2Farm: Nutrient Recycling—from pilot production to farms and fields” (Project ID: NWE601) and the Irish Research Council (Project ID: GOIPG/2020/99).

Data Availability Statement

The data presented in this study are available within the article.

Acknowledgments

We especially thank Cathal Redmond and John Murphy for their contributions to the experimental plots set-up, seasonal harvesting, sample processing, and fertiliser applications. We also thank the laboratory technical team at Teagasc Johnstown Castle Research Centre for processing samples for analysis.

Conflicts of Interest

The authors declare no conflicts of interest.

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Figure 1. Field experiment and sampling location (52°17′46.9″ N 6°30′32.1″ W); source: Geological Survey Ireland (GSI).
Figure 1. Field experiment and sampling location (52°17′46.9″ N 6°30′32.1″ W); source: Geological Survey Ireland (GSI).
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Figure 2. Effect of experimental treatments on the grass dry matter yield (DMY). Letters which differ within the sampling period indicate significant differences (p ≤ 0.05). Error bars are standard deviation (±SD) and n = 5. Treatments: NF, unfertilised control; SP 0, No P control (mineral NKS only); SP, P mineral control (mineral NPKS); CS, cattle slurry and mineral P control combination; PWS, potato waste struvite; MWS, municipal waste struvite; PLA, poultry litter ash; SSA, sewage sludge ash. MWS treatment was discontinued in 2021.
Figure 2. Effect of experimental treatments on the grass dry matter yield (DMY). Letters which differ within the sampling period indicate significant differences (p ≤ 0.05). Error bars are standard deviation (±SD) and n = 5. Treatments: NF, unfertilised control; SP 0, No P control (mineral NKS only); SP, P mineral control (mineral NPKS); CS, cattle slurry and mineral P control combination; PWS, potato waste struvite; MWS, municipal waste struvite; PLA, poultry litter ash; SSA, sewage sludge ash. MWS treatment was discontinued in 2021.
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Figure 3. Effect of experimental treatments on the annual P uptake by grass. Letters which differ within the sampling period indicate significant differences (p ≤ 0.05). Error bars are standard deviation (±SD) and n = 5. Treatments: NF, unfertilised control; SP 0, No P control (mineral NKS only); SP, P mineral control (mineral NPKS); CS, cattle slurry and mineral P control combination; PWS, potato waste struvite; MWS, municipal waste struvite; PLA, poultry litter ash; SSA, sewage sludge ash. MWS treatment was discontinued in 2021.
Figure 3. Effect of experimental treatments on the annual P uptake by grass. Letters which differ within the sampling period indicate significant differences (p ≤ 0.05). Error bars are standard deviation (±SD) and n = 5. Treatments: NF, unfertilised control; SP 0, No P control (mineral NKS only); SP, P mineral control (mineral NPKS); CS, cattle slurry and mineral P control combination; PWS, potato waste struvite; MWS, municipal waste struvite; PLA, poultry litter ash; SSA, sewage sludge ash. MWS treatment was discontinued in 2021.
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Figure 4. Pre- and post-harvest soil available phosphorus concentrations (Morgan’s P mg L−1) across treatments. Letters which differ within the sampling period indicate significant differences (p ≤ 0.05). Error bars are standard deviation (±SD) and n = 5. Treatments: NF, unfertilised control; SP 0, No P control (mineral NKS only); SP, P mineral control (mineral NPKS); CS, cattle slurry and mineral P control combination; PWS, potato waste struvite; MWS, municipal waste struvite; PLA, poultry litter ash; SSA, sewage sludge ash. MWS treatment was discontinued in 2021.
Figure 4. Pre- and post-harvest soil available phosphorus concentrations (Morgan’s P mg L−1) across treatments. Letters which differ within the sampling period indicate significant differences (p ≤ 0.05). Error bars are standard deviation (±SD) and n = 5. Treatments: NF, unfertilised control; SP 0, No P control (mineral NKS only); SP, P mineral control (mineral NPKS); CS, cattle slurry and mineral P control combination; PWS, potato waste struvite; MWS, municipal waste struvite; PLA, poultry litter ash; SSA, sewage sludge ash. MWS treatment was discontinued in 2021.
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Table 1. Chemical characteristics of mineral super phosphate, cattle slurry, struvite, and ash products.
Table 1. Chemical characteristics of mineral super phosphate, cattle slurry, struvite, and ash products.
Fertiliser and
Chemical Element		Super
Phosphate
(SP)		Cattle
Slurry
(CS)		Potato
Waste Struvite
(PWS)		Municipal
Waste Struvite
(MWS)		Poultry
Litter
Ash
(PLA)		Sewage
Sludge
Ash
(SSA)
TC (%DM)3.52 ± 0.5342 ± 2.360.44 ± 0.070.36 ± 0.061.16 ± 0.17<0.10
TN g kg−14.7 ± 0.9431.4 ± 1.6551.2 ± 0.2550.7 ± 0.210.2 ± 0.050.3 ± 0.18
P g kg−1167.0 ± 33.406.1 ± 0.13106.7 ± 0.82100.3 ± 2.9555.1 ± 5.8283.9 ± 2.36
K g kg−17.9 ± 1.5843.0 ± 0.3211.9 ± 0.070.6 ± 0.03106.7 ± 3.9212.6 ± 0.05
S g kg−118.0 ± 3.604.4 ± 0.110.1 ± 0.060.03 ± 0.0130.6 ± 1.2029.7 ± 1.11
Na g kg−13.0 ± 0.603.5 ± 0.010.1 ± 0.010.01 ± 0.0013.5 ± 0.79100.2 ± 1.34
Ca g kg−1212.0 ± 42.4031.7 ± 0.570.4 ± 0.140.27 ± 0.01155.6 ± 27.08103.4 ± 0.93
Mg g kg−13.8 ± 0.768.7 ± 0.0199.4 ± 0.8894.2 ± 2.7635.3 ± 1.8814.9 ± 0.23
Zn mg kg−1356.0 ± 71.2143.0 ± 1.304.1 ± 0.544.35 ± 5.251940.3 ± 42.71 *1797.3 ± 33.60 *
Fe mg kg−1914.0 ± 182.201756.0 ± 1561.7 ± 9.12277.5 ± 10.454632.7 ± 175.0259,622.1 ± 765.57
Cu mg kg−125.9 ± 5.1869.8 ± 1.100.5 ± 0.060.32 ± 0.13417.2 ± 3.72 *609.4 ± 4.01 *
Al mg kg−11900.0 ± 380.001321.0 ± 18539.9 ± 3.0634.5 ± 3.337459.5 ± 1227.7552,979.9 ± 295.65
Cr mg kg−194.5 ± 18.96.6 ± 0.402.8 ± 0.052.2 ± 0.1020.1 ± 1.50111.6 ± 3.41
Mn mg kg−153.1 ± 10.62218.0 ± 0.50128.3 ± 1.0949.2 ± 1.581915.4 ± 44.97955.0 ± 4.76
Ni mg kg−129.4 ± 5.883.8 ± 0.20<0.6<0.621.8 ± 0.51758.7 ± 1.87 *
Co mg kg−10.4 ± 0.081.6 ± 0.01<0.3<0.32.5 ± 0.5112.1 ± 0.55
Cd mg kg−117.8 ± 3.560.2 ± 0.03<0.15<0.151.0 ± 0.090.25 ± 0.02
Pb mg kg−1<2.0<2.0<2.0<2.037.2 ± 44.2419.7 ± 0.99
As mg kg−15.4 ± 1.08<1.5<1.5<1.5<1.5<1.5
Mo mg kg−113.4 ± 2.683.3 ± 0.10<0.5<0.512.4 ± 2.4215.5 ± 0.63
Abbreviations: TC, total carbon; TN, total nitrogen (Norg, NH4+, and NO3–); P, phosphorus, K, potassium; S, sulphur; Na, sodium; Ca, calcium; Mg, magnesium; Zn, zinc; Fe, iron; Cu, copper; Al, aluminium; Cr, chromium; Mn, manganese; Ni, nickel; Co, cobalt; Cd, cadmium; Pb, lead; As, arsenic; Mo, molybdate. * The concentration of the chemical element that exceeded the maximum EU-allowed concentration in the organic fertiliser [11]. In the RDFs and CS, a dispersion of data from their mean is expressed as standard deviation (±SD). In the SP fertiliser, a measurement uncertainty (±MU) is used to express the dispersion of the data from their mean.
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Karpinska, A.; Kakouli-Duarte, T.; Ashekuzzaman, S.M.; Byrne, J.; Schmalenberger, A.; Forrestal, P.J. Plant and Soil Effects of Alternative Sources of Phosphorus over Three Years of Application. Agronomy 2024, 14, 1591. https://doi.org/10.3390/agronomy14071591

AMA Style

Karpinska A, Kakouli-Duarte T, Ashekuzzaman SM, Byrne J, Schmalenberger A, Forrestal PJ. Plant and Soil Effects of Alternative Sources of Phosphorus over Three Years of Application. Agronomy. 2024; 14(7):1591. https://doi.org/10.3390/agronomy14071591

Chicago/Turabian Style

Karpinska, Anna, Thomais Kakouli-Duarte, S.M. Ashekuzzaman, John Byrne, Achim Schmalenberger, and Patrick J. Forrestal. 2024. "Plant and Soil Effects of Alternative Sources of Phosphorus over Three Years of Application" Agronomy 14, no. 7: 1591. https://doi.org/10.3390/agronomy14071591

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