Science of the Total Environment 799 (2021) 149424 Contents lists available at ScienceDirect Science of the Total Environment journal homepage: www.elsevier.com/locate/scitotenv Recovered phosphorus for a more resilient urban agriculture: Assessment of the fertilizer potential of struvite in hydroponics Verónica Arcas-Pilz a,1, Martí Rufí-Salís a,b,1, Felipe Parada a, Anna Petit-Boix c, Xavier Gabarrell a,b,⁎, Gara Villalba a,b a Sostenipra Research Group (SGR 01412), Institute of Environmental Sciences and Technology (CEX2019-000940-M), Z Building, Universitat Autònoma de Barcelona (UAB), Campus UAB, 08193 Bellaterra, Barcelona, Spain b Department of Chemical, Biological and Environmental Engineering, Universitat Autònoma de Barcelona (UAB), Campus UAB, 08193 Bellaterra, Barcelona, Spain c Chair of Societal Transition and Circular Economy, University of Freiburg, Tennenbacher Str. 4, 79106 Freiburg i. Br., Germany H I G H L I G H T S G R A P H I C A L A B S T R A C T • Struvite is tested in hydroponic produc- tion of Phaseolus vulgaris. • Yield, water fluxes, and P balances are analysed. • More yield is produced by plants with more than 5 g of struvite. • Slow release by struvite decreases the leached P. a r t i c l e i n f o a b s t r a c t Article history: Urban agriculture (UA) is a means for cities to become more resilient in terms of food sovereignty while shorten- Received 13 May 2021 ing the distance between production and consumption. However, intensive soilless UA still depends on the use of Received in revised form 28 July 2021 fertilizers, which relies on depleting non-renewable resources such as phosphorous (P) and causes both local and Accepted 29 July 2021 global impact for its production and application. With the aim to reduce such impacts and encourage a more ef- Available online 3 August 2021 ficient use of nutrients, this study assesses the feasibility of using struvite precipitated from an urban wastewater Editor: Damia Barcelo treatment plant as the unique source of P fertilizer. To do so, we apply various quantities of struvite (ranging from 1 to 20 g/plant) to the substrate of a hydroponic Phaseolus vulgaris crop and determine the yield, water flows and P balances. The results show that treatments with more than 5 g of struvite per plant produced a higher yield Keywords: (maximum of 181.41 g/plant) than the control (134.6 g/plant) with mineral fertilizer (KPO4H2). On the other Phosphorus hand, P concentration in all plant organs was always lower when using struvite than when using chemical fertil- Struvite izer. Finally, the fact that different amounts of struvite remained undissolved in all treatments denotes the impor- Fertilizer substitution tance to balance between a correct P supply to the plant and a decrease of P lost through the leachates, based on Circular economy the amount of struvite and the irrigated water. The findings of this study show that it is feasible for UA to effi- Industrial ecology ciently use locally recovered nutrients such as P to produce local food. Urban agriculture © 2018 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). ⁎ Corresponding author at: Department of Chemical, Biological and Environmental Engineering, Universitat Autònoma de Barcelona (UAB), Campus UAB, 08193 Bellaterra, Barcelona, Spain. E-mail address: xavier.gabarrell@uab.cat (X. Gabarrell). 1 These authors contributed equally to this research. https://doi.org/10.1016/j.scitotenv.2021.149424 0048-9697/© 2018 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). V. Arcas-Pilz, M. Rufí-Salís, F. Parada et al. Science of the Total Environment 799 (2021) 149424 1. Introduction °C) (Bridger et al., 1961) make it a slow-releasing valuable fertilizer that can reduce economic costs in agriculture (Rahman et al., 2014). Meeting the food demand of the ever-growing urban population is a However, only limited literature has explored the application of struvite global challenge. Since food provision to cities is highly dependent on in agricultural facilities. For example, Antonini et al. (2012), Uysal et al. long and complex supply chains, the distance between production and (2014), Gell et al. (2011) and Liu et al. (2011) assessed the maize perfor- consumption points has extensively increased. This prevents nutrient mance of struvite with different characteristics and origins in different recycling, while emitting huge amounts of greenhouse gases due to soils. In a review made by Li et al. (2019) we can see that almost all long-distance transport (Rees and Wackernagel, 1996; Thomaier et al., struvite trials found that vegetables grown with struvite had the same 2015). In this sense, moving towards more sustainable food systems -or even improved- performance compared to controls with conven- should be a priority in the following years (European Commission, tional fertilizers. 2020). To do so, alternatives that narrow the distance between produc- Creating a closed-loop, waste-to-resource system such as that of tion and consumption points have already been reported, being urban struvite recovery within the city limits and not applying it at this scale agriculture one of the most prominent (Deelstra, 1987). However, this seems contradictory within the concept of urban metabolism. In this implies that the resources required to produce food, mainly fertilizers sense, the synergy between struvite precipitation in urban WWTPs and water, must now be imported to cities. In the case of water, the and urban agriculture seems worth exploring considering the potential use of rainwater harvesting systems combined with hydroponics can of the latter to blur the lines between waste and resource within urban help meet the irrigation requirements without compromising the areas (Smit and Nasr, 1992; Ferreira et al., 2018; Rufí-Salís et al., 2020a). yield (Astee and Kishnani, 2010; Rufí-Salís et al., 2020b). On the other This article aims to assess the potential of struvite precipitated in a hand, the use of local fertilizers is still very limited, and often reduced WWTP as a fertilizer within the framework of urban metabolism. to the use of compost (Thomaier et al., 2015). The vertical and soilless Based on experimental and analytical results performed on a Phaseolus production systems have been reported to maintain greater yields vulgaris crop grown in a hydroponic rooftop greenhouse, we determine while at the same time avoiding land occupation making it a viable al- the implications of fertilization with struvite in terms of yield, water ternative while in some cases environmentally better than open field flows and P balances and provide recommendations to further improve production (Romeo et al., 2018). On the other hand the extensive use the performance of this waste-to-resource fertilizer. of mineral and synthetic fertilizers is necessary, causing potential and additional environmental damage in urban ecosystems if UA continues 2. Methodology growing without the search for alternative fertilization methods (Sanjuan-Delmás et al., 2018; Rufí-Salís et al., 2020c; Kwon et al., 2021). 2.1. Characterization of the system The case of phosphorus (P) fertilizers is of great relevance, since P is primarily obtained from non-renewable phosphate rocks. Moreover, The present study was conducted in a rooftop greenhouse on the previous studies quantify that 80% of the available stock of phosphate ICTA-ICP building, located in the campus of the Universitat Autònoma rocks is being used in the production of fertilizers (Shu et al., 2006). de Barcelona, 15 km away from Barcelona. The building is equipped Since half of the world's current economic phosphate resources will with a 900m2 rainwater harvesting system that stores water in a have been used up by the end of the 21st century (Steen, 1998; 100m3 tank. Most of this rainwater is used in the rooftop greenhouse Cordell et al., 2009) the European Union recognizes P as a critical re- (122.8m2) to irrigate crops with a hydroponic system, i.e. mixing source (European Comission, 2014). Among its recommendations, a water with nutrients before providing the solution through a dripping planned amendment of the fertilizer regulation encourages P recovery system (2 L/h) to the perlite substrate bags (40 L capacity). The perlite from local sources by enforcing a shift towards a more circular use of nu- substrate has a pH of 7, an electrical conductivity of 0.09 dS·m−1, a trients (European Comission, 2016). granulometry of [0–6] mm and 4 plants can be planted in each bag. In this sense, urban wastewater treatment plants (WWTPs) are well-known sources of secondary P. WWTPs have already been ad- 2.2. Fertilization and experimental set-up dressed as a potential alternative to importing mineral fertilizers (e.g. de-Bashan and Bashan, 2004; Kern et al., 2008; Shu et al., 2006). Struvite granules were obtained from Aarhusvand A/S company Struvite, also known as magnesium ammonium phosphate (MAP with from Aarhus, Denmark. This company distributes fertilizer grade the formula NH4MgPO4·6H2O) is a crystalline precipitate that has struvite under the name PhosphorCare™, recovered using the been gaining popularity as a way to recover P from wastewater. To in- Phosphogreen™ technology (Suez, 2018; Chrispim et al., 2019; Hall duce its precipitation a molar ratio of 1:1:1 for magnesium (Mg2+), am- et al., 2020; Muys et al., 2021). This technology is based on a fluidized monium (NH+ 3− 4 ) and phosphate (PO4 ) is needed, under specific pH bed reactor that creates the specific conditions to precipitate struvite conditions (8.5–9.5) (Buchanan et al., 1994; Bouropoulos and through the addition of magnesium chloride, sodium hydroxide and Koutsoukos, 2000; Le Corre et al., 2009). Originally the precipitation of air. The final struvite granules have a size range of 0.5–1.5 mm. struvite was associated to a major concern in WWTP being the cause Common bean plant (Phaseolus vulgaris var. Pongo) was chosen as of equipment damaging causing labor and infrastructure costs the crop for this study, planting nursery plants (approximately 10–14 (Borgerding, 1972; Doyle et al., 2003; Stratful et al., 2004). Struvite days old). To apply the struvite to the plants, we considered different forced precipitation has gained attraction since the 90's, not only to possibilities. Mixing it with the nutrient solution was discarded because avoid infrastructure damage but also as a P recovery technique (Doyle the system could not benefit from the slow-release characteristics of et al., 2003). This process has been studied and improved in the past struvite. Thus, we choose to directly apply the granules to the plant years making it a more efficient precipitation process (Le Corre et al., roots. Considering this option, we designed a system that consisted on 2009; Sena and Hicks, 2018; Li et al., 2019). Although the production mixing perlite with struvite inside a low-density polyethylene perfo- of struvite is gaining popularity, its commercial production is still scarce. rated bag with holes of no more than 1 mm diameter (Fig. SM1 in the The potential of P delivery of a WWTP in the form of struvite in the sys- Supplementary materials). At the same time, this system allows the in- tem where this study is located has been previously quantified by Rufí- teraction between struvite granules and roots and avoids the loss of un- Salís et al. (2020a), demonstrating the potential of these widespread in- dissolved struvite into the leachates due to draining through the perlite stallations to provide this ill distributed resource. bag. In terms of application, the properties of struvite as an effective Two different experiments were carried out: the validation test and source of nutrients (P-PO3− + 4 , N-NH4 and Mg-Mg 2+ ) for plants (Li and the determination test, both of them using double growing lines with 8 Zhao, 2003) and its low solubility in water (0.018 g·100 mL−1 at 25 substrate bags each (Figs. SM2 and SM14 in the Supplementary 2 V. Arcas-Pilz, M. Rufí-Salís, F. Parada et al. Science of the Total Environment 799 (2021) 149424 materials). The validation test served as a previous experimental set-up The measured P content of beans was multiplied by the measured to determine if the proposed methodology was functional and correct rates of biomass production to estimate the rate of P accumulation in possible influencing variables in the experiment, such as the use of the crop biomass. plastic bag to retain the struvite close to the plant rhizosphere or to scale the most suitable quantities of struvite for the determination 2.4. Validation test set-up and justification test. On the other hand the determination test was designed with the previous experience of the validation test. For control treatments, the From September 13th to December 3rd, 2018, 10 double growing nutrient solution applied to the crops in milligrams per litre was lines were used (totalling 320 plants), distributing the treatments as KPO4H2 – 136, KNO3 – 101, K2SO4 – 217.5, Ca(NO3)2 – 164, CaCl2 · showed in Fig. SM2 of the Supplementary material. The aim of this ex- H2O – 111, Mg(NO3)2 – 148.3, Hortilon – 10, and Sequestrene – 10. In periment was to validate and keep track of different parameters of the treatments with struvite, the mineral P source, KPO4H2 in this case, system, like for instance, make sure that the small, perforated bag did was excluded from the initial nutrient solution. All other mineral fertil- not have negative consequences on the crop development. To do so, izers were maintained. we split the control lines into two different treatments, VCB and VC0, using standard nutrient solution with and without the bags, respec- 2.3. Phosphorus balances tively. Secondly, to check the correct development of bean plants with struvite in a hydroponic system, we applied different struvite amounts To account for the P balances, Eq. (1) was calculated on a plant basis per plant: 5, 10, 15, 20 and 25 g corresponding to the treatments tagged for every control and struvite treatment. Fig. SM1 in the Supplementary as V5, V10, V15, V20 and V25, respectively. Additionally, a treatment material shows a diagram of the perforated bag with the elements with no struvite was tagged as V0. These amounts of struvite were displayed in Eq. (1). based on previous experiments done with the same crop species and variety in hydroponic cultivation that accounted for P uptake (Rufí- P NS þ P SI ¼ P LV þ P ST þ P BN þ P SF þ P LIX þ P AC ð1Þ Salís et al., 2020c). One week after the first harvest, KPO4H2 was added in the nutrient solution of struvite treatments until the end of In Eq. (1), P represents mass of phosphorus. PNS is the amount of the harvest to ensure a good nutrition to the plants during the produc- mineral P supplied through the irrigation system during all the crop tion period, which is highly demanding in P (e.g. Bender et al., 2015; cycle. PSI is the amount of P in the form of struvite applied at the begin- Kouki et al., 2016; da Silva et al., 2019). ning of the test. PLIX is the amount of P in the leachates during all the crop cycle. PLV, PST, and PBN, represent P uptake by leaves, stem and 2.5. Validation test results beans, respectively. PSF is the amount of remaining undissolved P in the form of struvite at the end of the test, plus the P adsorbed in the per- 2.5.1. Production and phenological stages lite granules. Finally, PAC is the amount of dissolved P accumulated in the The production results for the control treatments VCB and VC0 water retained in the substrate at the end of the crop. Three different showed that the perforated bag did not have any effect on the correct biomass and substrate sampling dates were used in every test: 26, 54 crop development and yield (Figs. 1 and SM5), as the yields from the dif- and 78 days after planting (DAP) for the validation test and 23, 51 and ferent lines do not differ between them (VC0_2 187.54 ± 69.35; VCB_1 72 DAP for the determination test. 186.15 ± 84.01 g/plant). Even though treatment VC0_1 generated more The initial nutrient concentration of the substrate was verified to be yield (224.84 ± 91.84 g/plant), it could be attributed to the fact that it negligible at the beginning of the experiment through atomic spectros- was an exterior cropping line facing the border and thus received copy and elemental analysis. Samples of the fertilizer solution were col- more radiation. Similarly, VCB_2 also produced more yield (195.45 ± lected directly from the drippers placed in the perlite bags. Leachate 88.63 g/plant) than its replicate (VCB_1) although no significant differ- samples were taken from plastic drainage buckets placed on one side ences where determined by the end of the experiment. of each line. To determine the PNS and PLIX, the respective samples On the other hand, treatments with struvite (Figs. SM3 and SM4 of were collected three times per week and externally analysed using the Supplementary material) exerted a similar yield than the control ICP-OES atomic spectroscopy (Optima 4300DV by Perkin-Elmer). PSI treatments at the end of the crop. The treatment with the highest quan- was quantified summing the amount of perlite in a specific bag with tity of struvite (V25) had the highest production median (203.85 g/ the amount of struvite that was applied, considering weights obtained plant), while the treatment with the lowest quantity of struvite (V5) by drying two struvite samples and two perlite samples at 105 °C in a had the highest mean (216.15 ± 93.54 g/plant). On the other hand, furnace until reaching constant weight (reached after 3 days). PSF was the treatment without struvite produced a really low yield (7.19 ± quantified differently in each test. In the validation test, all 4 samples 4.49 g/plant). for a specific treatment were homogenized after extracting the roots, The similarities in terms of yield between all struvite treatments at using distilled water to separate the struvite granules from the roots. the end of the cycle may be related to the addition of KPO4H2 fertilizer After this process, two random samples were dried at 105 °C in a furnace during the production phase. Moreover, we can see that struvite treat- until reaching constant weight, then grounded and digested with con- ments produced more than the control in the first 3 harvests (35, 39 centrated HNO3 in a Single Reaction Chamber microwave and exter- and 42 DAP) (Fig. SM6 in the Supplementary material). This effect is nally analysed using ICP-OES atomic spectroscopy. On the other hand, similarly observed for the phenological stages (Figs. 2 and SM7 to in the determination test, roots were shredded, homogenized and inte- SM10 in the Supplementary material). For the parameters that were grated within every individual substrate sample. Then, a fraction of quantified in different dates (number of leaves (Fig. 2), side shoots these samples was dried and analysed using the same method as in (Fig. SM7), open flowers (Fig. SM8) and floral buttons (Fig. SM9)), we the validation test. can see that the treatments with struvite not only had a correct early PLV, and PST were determined based on the nutrient content of every stage development, but also develop plant organs earlier than in control plant separately. Leaves and stem were separated, sorted into paper en- treatments. velopes and dried in a furnace at 65 °C until reaching constant weight (reached after 7 days), grounded and digested with concentrated 2.5.2. Water HNO3 in a Single Reaction Chamber microwave before analyzing exter- We applied more water in struvite treatments (125 L/plant) than to nally the concentration of P through ICP-OES atomic spectroscopy. The the control (94.76 L/plant) to ensure a proper dissolution of this fertil- same methodology was applied to determine the PBN, with randomly izer (Fig. SM11 – Supplementary material). However, we can see in chosen 500-gram bean samples being processed for every treatment. Fig. SM12 in the Supplementary material that if a greater amount of 3 V. Arcas-Pilz, M. Rufí-Salís, F. Parada et al. Science of the Total Environment 799 (2021) 149424 Fig. 1. Production (g/plant) of the control treatments in the validation test, with (VCB) and without (VC0) perforated bags for each harvest. Each panel in the figure grid represents the result for a harvesting day, with a total of 8 days (35 to 78 days after planting). Same letters (a,b) indicate no significant difference (p > 0.05) between treatment for each harvest time. Sample size for harvests 1, 2, 3, 4 and 5 (35- 54 DAP) corresponds to n = 28 plants, for harvests 6, 7 and 8 (63–78 DAP) n = 24 plants per treatment. Fig. 2. Number of leaves per plant per treatment and Days after Transplanting (DAP) in the validation test (13, 20, 27, 34 DAP). Same letters (a, b, c, d, e, f, g) indicate no significant difference (p > 0.05) between treatment for each counting time. Sample size n = 32 for each treatment. 4 V. Arcas-Pilz, M. Rufí-Salís, F. Parada et al. Science of the Total Environment 799 (2021) 149424 water flow through the perlite bag is provided through a greater irriga- between the treatments was marked with different letters in each plot. tion, leachates emitted by the struvite treatments with higher concen- All statistical analyses were made with the R studio software. trations (28.9 mg/L – V25) of this fertilizer tend to be similar to those of the control treatments. Obviously, this behaviour can only be ob- 3. Results served before the irrigation with mineral P added during the harvesting process. Similarly, we can see that the perforated bag mechanism did 3.1. Yield not affect the P concentration in the leachates between the control treatment C0 and CB. Figs. 3 (and SM15 and SM16 in the Supplementary material for the final total yield) shows the results of the accumulated yield per number 2.5.3. Phosphorus content of harvests, being the sixth harvest (71 DAP) the final one before Fig. SM13 of the Supplementary material shows the total P content uprooting the plants. Only treatments S1 (78.9 g/plant) and S2.5 in the different plant organs as well as the content in the substrate, de- (128.1 g/plant) had lower yields than the control treatment (134.6 g/ scribed as “undissolved”. P content in the stem show low variability plant), the first being significantly lower. On the other hand, all other along all treatments, with V25 having the highest (0.083 ± 0.020 g treatments with 5 g of struvite or above produced more than the control P) and V0 the lowest (0.008 ± 0.002 g P) at the end of the crop cycle. treatment, demonstrating the potential of struvite to produce similar or A great P accumulation was observed in the low production of the V0 even higher yields than with mineral fertilizer, as reported by Li et al. treatment with a content of 0.107 ± 0.005 g P (54 DAP) in beans, (2019). which was even higher than the highest observed in the control for As we can see in Fig. 3, it was not until the second harvest (42 DAP) VC0 (0.094 ± 0.013 g P –54 DAP), although the greater content was that great differences were observed between the S1 yield and the other found for treatment V25 with 0.172 ± 0.023 g P (54 DAP). The V0 treat- struvite treatments, while a decrease in S2.5 yield was observed be- ment doesn't show P results in leaves for 54 and 78 DAP because no tween the 4th and 5th harvest, 57 and 64 DAP, respectively. Regarding leaves remained in the plant at the sampling time. For this same reason, the control treatment, the first harvest produced lower yield (6.31 ± there is a lack of data in beans for 78 DAP. Finally, concentration in beans 5.71 g/plant) than the S5 (14.97 ± 11.91) struvite treatment being for struvite treatments was similar to the one observed in the control. even similar to the treatments with the lowest struvite application S1 For all plant organs, a pattern in the accumulation of P in the plant tissue (9.98 ± 8.51 g/plant). can be observed. In the first sampling all treatments show a rather low This fact reinforces the idea that the application of struvite could be accumulation with greater content for plants with greater struvite beneficial for early stage plant development, as the validation test quantities, in some cases also for the control treatments. For the second showed better behaviour in struvite than in control in phenological var- sampling, a bigger content difference can be seen with an acute increase iables. This fact could be related to the NH+ 4 supply by struvite, which of the V25 P content, especially for the stems and leaves. Finally, at 78 could benefit the plant root balance when combined with nitrate supply DAT, these differences between treatments even out and only treatment (Marschner, 1995). The fact that previous literature suggests that NH+ 4 V0 remains significantly reduced. This last part however, does not corre- supply to common bean could be harmful for plant development spond to the undissolved P in the perlite, where the P content in the (Chaillou et al., 1986; Guo et al., 2007) could be related to the amount substrate directly responds to the amount of struvite given, being al- of NH+ 4 supplied. Because struvite does not only enable a slow release ways higher for the V25. The control treatments receive the P through of P but also of NH+ + 4 , reaching NH4 accumulation to harmful levels irrigation making the existing content in the substrate comparably seems improbable. small. In terms of distribution, yields show an asymptote behaviour among treatments, where S20 produces the highest yield (g/plant) (181.41 ± 66.16) and S1, the lowest (78.94 ± 34.23). Fig. SM15 in the Supplemen- 2.6. Determination test set-up tary material shows how treatment S10 was detected as the exception for this tendency in terms of mean production (150.50 ± 56.10), prob- From September 16th to November 27th, 2019, 8 double growing ably related to bias parameters like shapes in the greenhouse or a non- lines were used (totalling 256 plants), distributing the treatments as homogenic distribution of struvite in the perlite bag. However, boxplots showed in Fig. SM14 of the Supplementary material. The determination represented in Fig. SM16 shows how the median of the final amount of test was designed based on the results of the validation test. The treat- yield harvested for S10 (155.70) follows the tendency, while not pre- ment distribution was randomized throughout the Greenhouse senting outliers in the distribution. avoiding the influence of climatic conditions. Thus, the struvite treat- ments were recalculated, applying per plant: 1, 2.5, 5, 7.5, 10, 15 and 3.2. Water 20 g corresponding to the treatments tagged as S1, S2.5, S5, S7.5, S10, S15 and S20, respectively. Struvite amounts below 5 g were applied Fig. SM17 of the Supplementary materials shows that the irrigated based on the yield and P content performance in the validation test for water in the control and the struvite treatments was the same (42.5 L V5. Since we found that the perforated bag did not affect plant develop- per plant), while Fig. 4 shows the accumulated P during the entire ment, we only used one control treatment, tagged as CB, which used the cycle in the different water streams. The quantity of P present in the same perforated bag as the struvite treatments. Moreover, considering control streams is much bigger than the one in the struvite streams, the yield and phenological findings in the validation test, we decided with the former irrigating and leaching 2.07 and 1.41 g of P per plant not to apply mineral P fertilizer to the struvite treatments at any for the entire crop cycle, respectively. The fact that the P leachates are point, so that struvite is the only source of P to the plants. one order of magnitude smaller when using struvite (maximum of 0.03 g of P per plant in S20) could be related to the slow-release charac- 2.7. Statistical analysis teristic of struvite reported in the literature. A clear benefit of this find- ing is a decrease in both P depletion and freshwater eutrophication The analysed data were tested for normality using the Shapiro-Wilk related to the leachates flow. Moreover, if the leachates of struvite treat- test p > 0.05. Further on, the Levene's test p > 0.05 was used to deter- ments do not contain a large amount of P, it means that most of the mine homogeneity of variance. Once these parameters were validated struvite has been whether taken up by the plant or remains undissolved the Duncan's multiple range test was used to assess the statistical signif- in the substrate. icance of treatments. On the other hand, non-parametric data were When comparing Figs. SM12 and SM18 of the Supplementary ma- analysed for significance using the Kruskal-Wallis test. The significance terial, we can see that P release by struvite is highly dependent on 5 V. Arcas-Pilz, M. Rufí-Salís, F. Parada et al. Science of the Total Environment 799 (2021) 149424 Fig. 3. Comparison of accumulated production of fresh bean per plant (g/plant) per treatment for each harvest time. Each panel in the figure grid represents the result for a harvesting day, with a total of 6 days (35 to 71 days after planting = DAP). Same letters (a, b, c, d) indicate no significant difference (p > 0.05) between treatment for each harvest time. Sample size for all harvests is n = 24 plants per treatment. the input water flow, represented in Figs. SM11 and SM17 for the val- the other hand, treatments S15 and S20 were the only struvite treat- idation and determination test, respectively. Because the volume of ments that did not stop emitting P to the leachates flow. irrigated water was three times less in the determination test (125.2 against 42.5 L per plant, respectively), the P observed in the 3.3. Substrate and undissolved struvite leachates is less than in the validation test, considering the period where P was not supplied through mineral fertilizer in the validation Fig. 5 shows the distribution of P among all possible input and out- test. puts considered in the system. At the end of the crop cycle, the control Differences are observed within the struvite treatments in Fig. 4, treatment supplied more P (2.07 g of P per plant) than the treatment highly dependent on the quantity of struvite that was applied at the be- with the highest amount of struvite (S20 - 1.90 g of P per plant). Most ginning of the crop. Treatments S1 and S2.5 stopped emitting P in the of the P supplied in the control treatments is discharged (68%), while leachates just 14 DAP, which could have triggered P deficiencies. On in the struvite treatments it still remains in the substrate. Fig. 4. Distribution of accumulated phosphorus in the irrigation and leachates of different treatments. Rcon: P in the control irrigation stream. 6 V. Arcas-Pilz, M. Rufí-Salís, F. Parada et al. Science of the Total Environment 799 (2021) 149424 3.4. Biomass Because the volume of irrigated water was three times lower in the determination test, the P observed in the leachates is lower than in the In terms of biomass, we can see that the concentration of P (in g per validation test, considering the period where P was not supplied kg) (Fig. 6) in all organs increases with the quantity of struvite applied through mineral fertilizer. Moreover, there is a significant amount of P to the treatment, having S15 and S20 similar concentrations in the accumulated in the substrate bag at the end of the treatment in the con- leaves (7.0 ± 1.3 and 6.7 ± 1.8, respectively) and stem (5.0 ± 0.9 and trol test. This stored P will be depleted if a successive crop is planted, 4.4 ± 1.2, respectively). However, the control treatment with mineral since the small nursery plants will not benefit from all of it due to the fertilizer presented higher concentrations of P than all struvite treat- lower needs of a smaller plant. With the addition of irrigation the accu- ments, also in beans (7.3 ± 0.4). This is especially relevant in the case mulated nutrients in the perlite bag would eventually be moved to the of beans, where the P deficiency in this organ directly affects the nutri- leachates. By applying struvite (and verified by the small amount of P tional value of the product that is going to reach the market. in the leachates in struvite treatments) this P is not stored and thus, not lost. 4. Discussion Based on the findings of this study, a well-designed struvite crop cycle needs to take into account two essential parameters. First, the Treatments S1 and S2.5 had lower yields than the control treat- quantity of struvite, considering that the quantity that remains undis- ments, establishing a clear relationship between the yield and possible solved at the end of the crop can be used again for a successive cycle. P deficiencies in these treatments. However, struvite remains undis- Second, the irrigation management, considering that if we modify this solved in all treatments, even though the production and the distribu- variable to increase the dissolution of struvite granules, we would also tion of P among plant organs was different between treatments be increasing the P in the leachates. Moreover, since previous studies (Figs. 3 and 6). The fact that we have undissolved struvite even in treat- highlighted the effect of the surface area of the granules on the solubility ments S1 and S2.5 shows that the limitation is not only related to the of slow-release fertilizers (Chien and Menon, 1995; Gell et al., 2011; Li quantity of struvite available, but also its dissolution (Figs. 4 and 6). et al., 2019), the size used in our study (0.5–1.5 mm) seems adequate While the struvite dissolution has been previously deemed to be due for the balance between P supply and P lost through the leachates. Liter- to the crystal granule size and placement (Talboys et al., 2016; ature with higher sizes reported solubility problems that affected early Degryse et al., 2017) previous literature fails to report the effect of the plant development (Talboys et al., 2016), while studies using lower irrigated water flow. Previous experiment on the struvite dissolution sizes or powder do not report these problems (Gell et al., 2011; in deionized water make clear that a greater dissolution can be ensured Antonini et al., 2012; Achat et al., 2014; Bonvin et al., 2015). Addition- with greater temperature and stirring energy as well as an acidic pH ally, the use of nursery plants is preferable since the struvite low disso- (Rahaman et al., 2006; Bhuiyan et al., 2007; Massey, 2007; Massey lution has been reported to be a disadvantage when providing P to feed et al., 2009; Ariyanto et al., 2017) reaching greater dissolutions close the transition from seeds to nursery plants (Talboys et al., 2016). to the commercial fertilizers. On the other hand the volume of water Struvite supply per plant should always be above 5 g for Phaseolus flows added to the crop has not been regarded as a determining factor vulgaris, considering that more quantity of struvite would release when granulated struvite is directly added to the substrate, especially more P into the leachates, but ensure that P is available for plants. On in hydroponic production. The obtained results in the present work the other hand, we should also account for the nutritional value of the shed light on the effect of the incoming irrigation on the struvite disso- beans, considering the ultimate function is to produce yield. In this lution as well as loss of P in the leachate. sense, P in the biomass was a variable where the control treatment Fig. 5. P distribution among all water, biomass and substrate compartment flows. This amount of struvite at the end of the crop could be recovered, or the same substrate with struvite could be used for a successive crop. 7 V. Arcas-Pilz, M. Rufí-Salís, F. Parada et al. Science of the Total Environment 799 (2021) 149424 Fig. 6. Phosphorus concentrations (g/kg) in the different treatments, separated by plant organ and days after planting (DAP). Same letters (a, b, c, d, e, f, g, h) indicate no significant difference (p > 0.05) between treatment for each harvest time. Sample size for all organs n = 4. Undissolved P content n = 2. had a better performance than struvite treatments. This uptake of sim- 5. Conclusions ilar P from struvite compared to soluble fertilizers has been previously reported by Ahmed et al. (2018) determining that different crops have On the way towards developing more circular economies in cities, a greater uptake of P while other have comparable or even lower the recovery of scarce resources that can be utilised within the urban growth. While Phaseolus vulgaris was not previously observed, a study boundaries will play an important role. This study assessed the perfor- with soybean was performed compared to the P uptake with triple su- mance of the potential application of struvite in hydroponic bean perphosphate (TSP). The resulting crops show a similar uptake of both crops to diminish the need for external resources in urban agriculture. P sources by the plant with different quantities of P applied Three main conclusions could be drawn from this analysis. (Thompson, 2013). The P uptake in Phaseolus vulgaris with the use of struvite compared to monopotassium phosphate can also be seen in First, applying struvite in hydroponics crops equals and even in- previous literature (Arcas-Pilz et al., 2021) although this experiment creases the yield compared to mineral fertilizer while diminishing also explores the use of rhizobium inoculation as substitute for the N P losses in the leachates, contributing to both less nutrient depletion fertilization, obtaining a general reduction of plant growth. It is also im- and eutrophication potential. In this sense, a quantity above 5 g/ portant to keep in mind that the quantity of applied struvite is 2 g and plant of struvite was observed to be enough for correct bean plant 5 g for the proposed treatments. Rech et al., 2018 also discusses the development and yield production. low solubility of struvite compared to TSP, also mentioning a greater up- Second, the input water flow was relevant in supplying enough P to take of P by soybean and wheat with struvite fertilization compared to the plants through dissolution using struvite. On the other hand, a the control treatment. correct water irrigation management is relevant to diminish P losses Only S15 and S20 reach a similar P amount to the control in all through overdissolution. Therefore, a balance between these two plant organs. For this reason, a quantity between 15 and 20 g of potential problems should be one of the key parameters when grow- struvite, a responsible irrigation management and growing succes- ing crops with struvite. sive crops with the same substrate constitutes the best option to Third, a great quantity of struvite remains undissolved at the end of grow a well-designed struvite bean crop cycle. the crop in all treatments. In this sense, planting a successive cycle or Although the P uptake of the struvite fertilized treatments appears to recovering the struvite of the substrate could be alternatives to avoid be equal or rather smaller than the control treatment the production is losing valuable nutrients. greater for all treatment with more than 5 g of struvite. In the literary re- view proposed by Ahmed et al., 2018 the increase of biomass and yield With the obtained information, it is adequate to say that the use of by plants fertilized with struvite can be related to the simultaneous dis- struvite in hydroponic production as a way to supply P is viable. Our solution of Mg and NH+ 4 . Although the uptake of P is reported in this study demonstrated that no special equipment or conditions were re- study the Mg and NH+ 4 concentration in the plant was not analysed. quired for the use of struvite in hydroponic production. The use of this The Mg uptake has been reported to be strongly correlated with the crystal therefore is strongly recommended and it extraction and use given Mg in the struvite and can be pointed out as a possible source rea- should be pursued for further optimization of the existing P sources. son for greater growth and production (Antonini et al., 2012; Ahmed Based on the findings presented in this paper, we believe that future et al., 2018; Rech et al., 2018). research should focus on three different aspects. First, the role of NH+ 4 8 V. Arcas-Pilz, M. Rufí-Salís, F. Parada et al. Science of the Total Environment 799 (2021) 149424 supplied by struvite on plant development during the first production Ariyanto, E., Ang, H.M., Sen, T.K., 2017. The influence of various process parameters on dissolution kinetics and mechanism of struvite seed crystals. J. Inst. Eng. (India) Ser. phase. Second, the performance of crops if successive cycles are grown A 98 (3), 293–302. https://doi.org/10.1007/s40030-017-0212-4 Springer India. using the same undissolved struvite in hydroponic systems. Third and Astee, L.Y., Kishnani, N.T., 2010. Building integrated agriculture: utilising rooftops for sus- finally, the modelling of P release of struvite based on quantity applied tainable food crop cultivation in Singapore. J. Green Build. 5 (2), 105–113. https://doi. org/10.3992/jgb.5.2.105 Allen Press. and input water flow. Bender, R.R., Haegele, J.W., Below, F.E., 2015. Nutrient uptake, partitioning, and remobili- zation in modern soybean varieties. Agron. J. 107 (2), 563–573. https://doi.org/10. CRediT authorship contribution statement 2134/agronj14.0435. Bhuiyan, M.I.H., Mavinic, D.S., Beckie, R.D., 2007. A solubility and thermodynamic study of struvite. Environ. Technol. 28 (9), 1015–1026. https://doi.org/10.1080/ All authors were responsible for the conception and design of the 09593332808618857. study. V. Arcas-Pilz, M. Rufí-Salís, A. Petit-Boix, G. Villalba and X. Bonvin, C., et al., 2015. Plant uptake of phosphorus and nitrogen recycled from synthetic Gabarrell conceived the original idea for the study. M. Rufí-Salís, V. source-separated urine. Ambio 44 (2), 217–227. https://doi.org/10.1007/s13280- 014-0616-6. Arcas-Pilz and F. Parada set up, supervised and acquired the data Borgerding, J., 1972. Phosphate deposits in digestion systems. J. Water Pollut. Control Fed. for the experimental tests. M. Rufí-Salís and V. Arcas-Pilz processed 44 (5), 813–819. and analysed the data. M. Rufí-Salís and V. Arcas-Pilz took the lead Bouropoulos, N.C., Koutsoukos, P.G., 2000. Spontaneous precipitation of struvite from aqueous solutions. J. Cryst. Growth 213 (3–4), 381–388. https://doi.org/10.1016/ in writing the manuscript. All authors critically revised the draft for S0022-0248(00)00351-1 North-Holland. important intellectual content. All authors gave their final approval Bridger, G.L., Salutsky, M.L., Starostka, R.W., 1961. Metal ammonium phosphates as fertil- to the manuscript. izers. 140th Meeting of the American Chemical Society, pp. 1–19. Chaillou, S., et al., 1986. Nitrate or ammonium nutrition in french bean. Plant Soil 91, 363–365. Declaration of competing interest Chien, S.H., Menon, R.G., 1995. Factors affecting the agronomic effectiveness of phosphate rock for direct application. Fertil. Res. 41 (3), 227–234. https://doi.org/10.1007/ The authors declare that they have no known competing financial BF00748312 Springer. Chrispim, M.C., Scholz, M., Nolasco, M.A., 2019. Phosphorus recovery from municipal interests or personal relationships that could have appeared to influ- wastewater treatment: critical review of challenges and opportunities for developing ence the work reported in this paper. countries. J. Environ. Manag. 248 (February), 109268. https://doi.org/10.1016/j. jenvman.2019.109268 Elsevier. Cordell, D., Drangert, J.O., White, S., 2009. The story of phosphorus: global food security Acknowledgements and food for thought. Glob. Environ. Chang. 19 (2), 292–305. https://doi.org/10. 1016/j.gloenvcha.2008.10.009. The authors are grateful to Universitat Autònoma de Barcelona for Le Corre, K.S., 2009. Phosphorus recovery from wastewater by struvite crystalliza- tion: a review. Crit. Rev. Environ. Sci. Technol. https://doi.org/10.1080/ awarding a research scholarship to M. Rufí-Salís (PIF-UAB 2017), to 10643380701640573 Taylor & Francis Group. the Spanish Ministry of Economy, Industry and Competitiveness De-Bashan, L.E., Bashan, Y., 2004. Recent advances in removing phosphorus from waste- (Spain) for the grant awarded to V. Arcas-Pilz (FPI-MINECO 2018), water and its future use as fertilizer (1997–2003). Water Res. https://doi.org/10. and to the National Commission for Scientific and Technological Re- 1016/j.watres.2004.07.014. Deelstra, T., 1987. Urban agriculture and the metabolism of cities. Food Nutr. Bull. 9 (2), search (Chile) for the grant awarded to F. Parada (PFCHA-CONICYT 1–3. https://doi.org/10.1177/156482658700900210. 2018 – Folio 72180248). This work was supported by the Spanish the Degryse, F., et al., 2017. Dissolution rate and agronomic effectiveness of struvite fertilizers “María de Maeztu” program for Units of Excellence in R&D [CEX2019- – effect of soil pH, granulation and base excess. Plant Soil. Plant Soil 410 (1–2), 139–152. https://doi.org/10.1007/s11104-016-2990-2. 000940-M]. A. Petit-Boix thanks the German Federal Ministry of Educa- Doyle, J.D., et al., 2003. Chemical control of struvite precipitation. J. Environ. Eng. 129 (5), tion and Research for the financial support of the research group 419–426. https://doi.org/10.1061/(ASCE)0733-9372(2003)129:5(419). “Circulus - Opportunities and challenges of transition to a sustainable European Comission, 2014. Critical raw materials. Internal Market, Industry, Entrepre- neurship and SMEs. circular bio-economy”, grant number 031B0018. European Comission, 2016. Paket zur Kreislaufwirtschaft. Verordnung des Europäischen The research leading to these results has received funding from the Parlaments und des Rates mit Vorschriften für die Bereitstellung von European Research Council under the European Horizon2020 research Düngeprodukten mit CE-Kennzeichnung auf dem Markt und zur Änderung der and innovation program under grant agreement No 862663 (FoodE) Verordnungen. 0084, p. 1069. European Commission, 2020. A Farm to Fork Strategy for a Fair, Healthy and as well as, ERC grant agreement n° 818002 URBAG, awarded to Gara Vil- Environmentally-friendly Food System, pp. 1–13 (February 2019). lalba. Finally we would like to thank Secretaria d'Universitats i Recerca Ferreira, A.J.D., 2018. Urban agriculture, a tool towards more resilient urban communi- del departament d'Empresa i Coneixement de la Generalitat de Catalu- ties? Curr. Opin. Environ. Sci. Health 5, 93–97. https://doi.org/10.1016/J.COESH. 2018.06.004 Elsevier. nya for the grand awarded under the n° AGAU 2020 PANDE 00021. Gell, K., et al., 2011. Safety and effectiveness of struvite from black water and urine as a The publication reflects the author's views. The Research Executive phosphorus fertilizer. J. Agric. Sci. 3 (3), p67. https://doi.org/10.5539/jas.v3n3p67. Agency (REA) is not liable for any use that may be made of the informa- Guo, S., et al., 2007. 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