Next Article in Journal
Deterministic and Probabilistic Assessment of Failure Mechanisms in Geosynthetic-Reinforced Embankments
Next Article in Special Issue
Impact of Fish, Mollusk and Seafood Consumption before Sample Donation on Urinary and Toenail Metal Levels in Workers Exposed to Heavy Metals
Previous Article in Journal
The Use of a Laser Diffractometer to Analyze the Particle Size Distribution of Selected Organic Soils
Previous Article in Special Issue
Risk Elements in Total Suspended Particles in Areas Affected by Opencast Mining of Brown Coal
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Applied Sciences
Volume 14
Issue 18
10.3390/app14188105
applsci-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Long-Term Amendment with Sewage Sludge: Effects on Nutrient Value and Trace-Metal Content in Different Parts of Maize Plants

by
Francesc Camps-Sagué
1,
Àngela Dolores Bosch-Serra
2,*,
Alicia Daniela Cifuentes-Almeida
2,
Montserrat Maria Boixadera-Bosch
2 and
Francesc Domingo-Olivé
1
1
IRTA Mas Badia, Agricultural Experimental Station Mas Badia, E-17134 La Tallada d’Empordà, Spain
2
Department of Chemistry, Physics, Environmental Sciences and Soil, University of Lleida, E-25198 Lleida, Spain
*
Author to whom correspondence should be addressed.
Appl. Sci. 2024, 14(18), 8105; https://doi.org/10.3390/app14188105
Submission received: 12 August 2024 / Revised: 31 August 2024 / Accepted: 7 September 2024 / Published: 10 September 2024
(This article belongs to the Special Issue Heavy Metal Toxicity: Environmental and Human Health Risk Assessment: Volume II)
Browse Figures
Versions Notes

Abstract

:
Agricultural soils play a key role in the achievement of a circular nutrient economy. The use of sewage sludges as fertilizers is important for such an achievement, assisting in the maintenance of soil health and nutritional crop value. This study was established, after 23 years of a fertilization experiment, in calcareous soil under a maize monoculture. The treatments included mineral fertilization as a control (MIN, 225 kg N ha−1) and two sludge treatments, where doses followed a threshold sludge nitrogen criterion (SNC, 170 kg org-N ha−1) or a threshold soil phosphorus criterion (SPC; when the soil Olsen-P value exceeded 40–60 kg P ha−1, the sludge application was stopped). A detailed study was performed on Cd, Cu, F, Mn, Pb, and Zn soil extractable with diethylenetriaminepentaacetic acid (DTPA), as well as the nutrient and heavy metal concentration of different fractions of the maize plant (grain, cob, and the rest of the plant). Extractions were also quantified. No biomass-yield differences were observed in the different parts of the maize plant in the year of sampling. Sludges increased the soil DTPA extraction of Cd, Cu, Fe, and Zn and diminished Mn extraction, without differences in extractable Pb. The SNC, when compared with MIN, showed increased P cob concentrations, and in grain, it showed increased Fe, Cr, and Co concentrations. The SPC figures of the studied parameters were, in general, between both treatments (MIN and SNC), although Cr extractions in grain diminished vs. SNC. Based on the results, the SPC can be recommended as it also avoids excessive available-P build up.

1. Introduction

The European Urban Waste Water Treatment Directive (UWWTD) from 1991, revised in 2022 [1], established treatment standards to better protect the environment from the adverse effects of wastewater discharges from urban sources and specific industries. The better recovery of nutrients is inherent to such treatments, while sludge management should be improved to better align with the principles of a circular economy (following article 4 of Directive 2008/08/EC). This Directive [2] aligns with the importance of the reuse and valorization of residues, which include sewage sludges (SSs). As all cities with more than 1000 inhabitants should implement wastewater treatments, the agricultural disposal of SS is a sound option due to the potential volume of SS generated. Also, SSs from rural areas have a lower content of heavy metals than those from industrialized areas [3]. In Spain, around 80% of SSs produced are reused as fertilizers [4].
The application of sewage sludge to land may introduce potential contaminants such as heavy metals. The soil behavior of heavy metals and the associated environmental risk assessment is highly related to soil pH [5]. It is accepted that their mobility is not important in calcareous soils [6], as trace elements are maintained in forms of low availability for cultivated plants, mainly under drought conditions [7]. Accordingly, the metal concentration in plants is mainly affected by soil typeto a greater extent than the SS dose [8]. Many field experiments are established on acid [9] or neutral [10,11] soils, or using acid soils under controlled conditions, usually with short crop cycles [12,13]. Moreover, some experiments in calcareous soils are short-term experiments [14] focused on crop quality [15]. There is therefore a lack of knowledge about crop composition related to the use of SS on soils of high pH. Furthermore, under field conditions, when SSs are applied to calcareous soils, an increase in the soil bioavailability of some trace metals, and also in barley concentrations, has been observed [16]. In a previous work, eight years before the current study, changes in soil heavy metals were also found, but they were far below the thresholds established by regulations and without changes in maize grain concentrations [17]. Maize is an interesting crop for SS studies as it produces high grain-biomass yields. Additionally, the rest of the plant and cob kernel can be reused for animal feeding [18], which means that the composition of maize parts, linked to SS use, is of interest in the context of a circular nutrient economy.
The limits of heavy metals in soil and sewage sludges (Cd, Cu, Ni, Pb, Zn, Hg, Cr (VI), and inorganic As) regarding their agricultural use are stipulated in the Spanish laws [19,20]. Legislation has been developed in order to avoid their excessive accumulation in soil. Furthermore, the EU [21] established a limit of As, Cd, Hg and Pb in animal feed and human food [22].
The official analytical methods used to quantify heavy metals in soil [20] are based on extraction with aqua regia [23]. However, the most available forms of different heavy metals in neutral and near-alkaline soils are considered to be those obtained through the diethylenetriaminepentaacetic acid (DTPA)-extractable soil fraction, mainly for Zn and Cu bioavailability [24].
The application of SSs, as organic fertilizers, is also based on N criteria according to plant demand and/or general restrictions on water quality protection across Europe. In the area of this study, restrictions on the available-P soil level also apply. The amount of 170 kg N ha−1 year−1 has been established as the maximum to be applied for water protection from organic fertilizers in nitrate-vulnerable areas. Also, an infraction threshold of 150 mg P kg−1 of available P (Olsen-P) and a warning level of 80 mg P kg−1 have also been set up in this Spanish region [25].
The objective of this work was to evaluate the advantages and potential constraints of 23 years of maize fertilization with sewage sludges (SSs) when compared with mineral fertilization, in a calcareous soil, and in the context of EU fertilization restrictions. This evaluation was focused (i) on Cu, Fe, Mn, Zn and Cd and Pb soil bioavailability, and (ii) on the concentrations of nutrients (N, P, K, Mg, S, Fe, Mn, Cu, and Zn) and other trace elements (Cd, Co, Cr and Pb) in different parts of maize crops (grain, cob and the rest plant), as well as the associated extractions. We hypothesized that a higher availability of some trace elements (micronutrients) will increase the general nutrient value of different maize parts for animal feeding. We also hypothesized that a potential increase in the rest of the trace-element concentrations (below legislation limits) will not reduce yields. The described advantages will be observed when fertilization with SS is based on nitrogen criteria, or even under more-restrictive use when phosphorus criteria are applied.

2. Materials and Methods

2.1. Site Description

This study was carried out in in the northwest of the Iberian Peninsula. The experimental field was established in 1996 and has since been maintained. It was devoted to a maize (Zea mays L.) monoculture. The coordinates of the site are 42°05′37″ N, 03°06′39″ E, with an altitude of 17 m a.s.l. The area has a dry Mediterranean climate, with an annual average precipitation of 646 mm year−1, with most rain falling during the first three months of autumn. Annual average temperature is 15 °C, and the highest temperatures are recorded in summer (23 °C on average). The annual average amount of reference evapotranspiration (FAO Penman–Monteith equation) is 977 mm.
The soil is very deep (>1.2 m), without coarse particles. It has been classified as an Oxyaquic Xerofluvent and the family particle-size class was coarse-loamy [26]. It has a pH of 8.2 (1:2.5 soil/water, potentiometry) and an electrical conductivity (1:5 soil/water) of 0.16 dS m−1. It is calcareous (140 g kg−1, equivalent calcium carbonate, Bernard’s calcimeter method) and without gypsum.

2.2. Experimental Design

The experimental area was divided into four blocks (replicates), and, in each block, three fertilization treatments were randomized. They included a mineral N treatment (MIN) and other two treatments with sewage sludges (SSs), which followed an N threshold criterion (SNC) or a P threshold criterion (SPC). The MIN treatment was used as a reference; it received 100 kg ha−1 of N, P2O5 and K2O at maize sowing, applied as a triple 15 complex fertilizer, and it was complemented by an additional application of 70 kg N ha−1 at topdressing as ammonium nitrate. In the SPC and SNC treatments, sludge was applied at a rate of 170 kg N ha−1 with a mineral supplementation of 100 kg K2O ha−1. However, in the SPC treatment, when soil Olsen-P levels exceeded 40–60 mg P kg−1, no sludge was applied the following season; instead, N and K mineral fertilizers were applied at similar rates to the MIN treatment. In accordance with this criterion, no sludge was applied from 2006 to 2009 in SPC, nor in 2014. The plots undergoing sludge fertilization had a size of 41 m2 (9.6 m long × 4.25 m wide), while MIN plots had an area of 81.6 m2 (9.6 m long × 8.5 m wide).
Anaerobically digested sludge came from a village with a population of around 18,000 inhabitants, mainly devoted to tourism activities. Sewage sludges were spread over the soil surface one month before maize sowing, and they were buried by disk-ploughing (~0.2 m depth). Heavy-metal concentrations in sludge for use in agriculture were always below the allowed concentrations [12].
The present study was performed in 2019, 23 years after the experiment’s establishment. The historical average grain yield (14% humidity) was 14 Mg ha−1 (coefficient of variation of 7%), without significant differences between treatments [27]. In the previous harvest (10 October 2018), maize stalks were chopped and incorporated into the soil through ploughing. In 2019, maize (P1570Y—Pioneer, Corteva; Madrid, Spain) was sowed on 12 April (80,000 seeds ha−1), and it was harvested on 10 October. Plots were irrigated by a high-frequency system (with drippers separating every 0.40 m in the line, and one line was established every two rows of maize). The amount of water applied between early June and mid-September was 3936 m3 ha−1. Daily irrigation was calculated from a soil water balance. The evapotranspiration of a reference crop (ETo, Penman–Monteith formula) was obtained from an automatic meteorological station located 200 m from the experimental field. ETo values were adjusted according to the phenology of the maize crop by multiplying by a coefficient that ranged from 0.3 to 1.1. If the daily recorded precipitation was higher than 3 mm, the effective precipitation was obtained by multiplying the recorded precipitation by 0.8.

2.3. Field Samplings and Analytical Methods

On 5 October 2018, soil was sampled at a depth of 0–0.2 m to obtain a more detailed chemical characterization (Table 1). Composite soil samples from the three blocks and treatment were stored in polyethylene bags protected from sunlight and immediately transferred to the laboratory. They were dried at room temperature, and the fine fraction (apparent diameter < 2 mm) was obtained after sieving. Oxidizable organic carbon was determined following the methodology described in Walkley and Black [28], and available P content was determined using the Olsen method (sodium bicarbonate-extractable P at pH 8.5) [29]. Available K was obtained by extraction with ammonium acetate 1N (pH = 7) [30] and quantified by atomic absorption spectrophotometry; the AAnalyst 200 analyzer (PerkinElmer, Shelton, CT, USA) was used. Total heavy metals were analyzed according to the UNE-EN 16174:2012 procedure [31].
Furthermore, from additional samples in each plot, extractable Fe, Zn, Mn and Cu (microelements) plus Cd, Cr and Pb were obtained with a one-step extraction method with 0.005 M diethylenetriaminepentaacetic acid (DTPA) solution (1:2, w:v), as described in [32]. This extraction procedure focuses on detecting trace metals in the most labile fractions of the soil, which can lead to their potential absorption by plants [33], and it was especially developed for calcareous soils. The mentioned elements were quantified using inductively coupled plasma-mass spectrometry (ICP-MS) in a 7700x analyzer (Agilent Technologies, Santa Clara, CA, USA), following the standard [34].
A sludge sample was taken every season before the application of the organic fertilizer; this was to adjust the rate of N to 170 kg N ha−1 through an analysis in the laboratory using the Kjeldahl digestion and distillation method [35]. In 2019, the total N in sewage sludges was 61.2 g kg−1 over dry matter. Total carbon was determined by ignition at 550 °C. Heavy metals, P and K in sludges were analyzed from microwave-digested samples [23] with aqua regia (3:1, v:v, HCl:HNO3) and quantified using inductively coupled plasma-mass spectrometry, as explained previously.
In the 2019 maize harvest, plants from 0.75 m2 of each plot (central part) were harvested and divided into three parts: the grain, the cob and the rest of the plant biomass. The different parts were weighed, dried, ground, digested and analyzed. From microwave-digested samples [23] using HNO3 and H2O2 (3:2:2, v:v:v, HNO3:H2O2:H2O) [36], Mn, Cr, Cd, Co, Pb were analyzed, while P, K, Mg, S, Fe, Zn, Cu were determined using HNO3 and HCl (3:1:1, v:v:v, HNO3:HCl:H2O) [37]. All these elements were quantified using inductively coupled plasma-mass spectrometry, as indicated previously.

2.4. Statistical Analyses

The statistical analyses were carried out using the SAS statistical package v9.4 [38]. Data were subjected to appropriate analysis of variance (ANOVA) according to the experimental field design (Table A1, Table A2, Table A3, Table A4, Table A5, Table A6, Table A7, Table A8, Table A9, Table A10, Table A11, Table A12, Table A13, Table A14, Table A15 and Table A16). When the ANOVA analysis detected significant differences, a separation of means was performed according to Duncan’s multiple-range test (DMRT) for α = 0.05.

3. Results

The initial values of Olsen-P and total Cd, Cu, Cr, Pb and Zn (Table 1) from the composite samples were below the limits of 150 P kg−1, 1.5 mg Cd kg−1, 100 mg Cu kg−1, 100 mg Pb kg−1 and 200 mg Zn kg−1 established by [11,12,39]. In all treatments, values of hexavalent chromium, mercury, selenium and silver were lower than 0.5 mg Cr (VI) kg−1, 0.4 mg Hg kg−1, 1.5 mg Se kg−1 and 5.0 mg Ag kg−1, respectively, which also satisfied the legislation.
Fertilization treatments did not affect soil Pb availability (DTPA extraction), with average values of 1.9 mg Pb kg−1, while they did for Cd, Cu, Fe, Mn and Zn (Table A1). Sewage sludges increased Cd, Cu and Fe availability in the soil when compared with MIN treatment. Availability ranged from 52 to 57 µg Cd kg−1, from 8.5 to 11.6 mg Cu kg−1 and from 11.4 to 19.9 mg Fe kg−1. The availability of Zn increased in the following order: MIN< SPC < SNC treatments, from 1.9 to 4.6 mg Zn kg−1, while Mn availability increased following an inverse order, from 6.1 mg Mn kg−1 in SNC to 7.9 mg Mn kg−1 in MIN (Figure 1).
The yields of the grain, the cob and the rest of the plant biomass were not significantly different based on the fertilization treatments applied (Table A2). The average biomass yield values were 13,779, 2293 and 11,024 kg ha−1 for the grain, the cob and the rest of the plant, respectively (Figure 2).
Concentrations and fractionated extractions for maize are presented in Figure 3 and Figure 4, respectively. The concentrations of Cr, Co and F in grain; concentrations of P and Mn in the cob; and concentrations of Cr, Co, and Pb in the plant were statistically different with the fertilization treatments, but no differences were found for the rest of the analyzed elements in the different parts of maize plants (Table A3, Table A4, Table A5, Table A6, Table A7, Table A8 and Table A9; Figure 3).
In grain, the SNC showed the highest values in chrome concentration (1.5 mg Cr kg−1, Figure 3d) and iron (33.6 mg Fe kg−1, Figure 3c), but it only differed from MIN in cobalt concentrations (26.1 and 9.5 mg Co kg−1 for SNC and MIN, respectively; Figure 3e).
Phosphorus (Figure 3b) and manganese (Figure 3c) concentrations in cobs were lower in the MIN treatment than for the SNC and SPC. In cobs, P values ranged from 0.59 to 0.80 mg P kg−1, while in Mn, they ranged from 6.4 to 7.2 mg Mn kg−1.
In the rest of the plant, Co (Figure 3e) and Cr (Figure 3d) concentrations were lower for the SPC than in the rest of treatments. Concentrations ranged from 79 to 100 µg Co kg−1, while in Cr, they ranged from 0.32 to 0.51 mg Cr kg−1. Also, for the rest of the plant, Pb concentrations (Figure 3e) were lower in the SCP (228.6 mg Pb kg−1) than in MIN (283.2 mg Pb kg−1) and SNC (288.5 mg Pb kg−1).
For the rest of concentrations analyzed, without significant differences between fertilization treatments (Table A3, Table A4, Table A5, Table A6, Table A7, Table A8 and Table A9; Figure 3), the average values (± standard deviation) for grain were 12.1 g N kg−1 (±0.4), 4.2 g K kg−1 (±0.1), 2.7 g P kg−1 (±0.1), 1.3 g Mg kg−1 (±0.04), 1.3 g S kg−1 (±0.1), 5.2 mg Mn kg−1 (±0.3), 22.8 mg Zn kg−1 (±1.4), 3.1 mg Cu kg−1 (±0.1), 12.2 µg Pb kg−1 (±2.7) and 1.4 µg Cd kg−1 (±0.2). For cobs, the average concentration values (±standard deviation) were 7.9 g N kg−1 (±0.8), 11.0 g K kg−1 (±0.7), 0.6 g Mg kg−1 (±0.1), 0.7 g S kg−1 (±0.05), 29.0 mg S kg−1 (±2.0), 32.0 mg Zn kg−1 (±7.5), 3.1 mg Cr kg−1 (±0.2), 3.4 mg Cu kg−1 (±0.1), 31.5 µg Co kg−1 (±2.0), 24.3 µg Pb kg−1 (±1.8) and 16.0 µg Cd kg−1 (±8.9). For the rest of the plant, the average concentration values (±standard deviation) were 4.9 g N kg−1 (±0.7), 15.4 g K kg−1 (±0.3), 1.2 g P kg−1 (±0.5), 1.6 g Mg kg−1 (±0.2), 1.0 g S kg−1 (±0.1), 222.4 mg Fe kg−1 (±27.7), 39.2 mg Mn kg−1 (±10.0), 17.5 mg Zn kg−1 (±7.0), 4.1 mg Cu kg−1 (±0.1) and 12.2 µg Cd kg−1 (±2.7).
Extractions diminished for the SPC treatment when compared with MIN in grain N (23 kg N ha−1) and cob Cd (6 mg Cd ha−1) (Figure 4a,f). The SNC treatment, when compared with MIN, reduced grain S (Figure 4b) and cob Cd (Figure 4f) extractions by 2 kg S ha−1 and 5 mg Cd ha−1. No differences were found in the fractioned maize extractions of the rest of elements (K, P, Mg, Cu, Mn, Fe, Zn, Co and Pb) (Figure 4).

4. Discussion

The obtained grain yields (Figure 2) were in accordance with the historical average of 14 Mg ha−1 [19], without differences between fertilization treatments. From the initial framework (Table 1), we observed the tendency of Olsen-P soil levels to increase with SSs compared with mineral fertilization (Table 1). This tendency is consistent with [40], as sewage sludges usually have high P content related to N. This initial higher P concentration due to the application of organic materials is also supported by the findings of [41], when organic fertilization was based on N criteria. However, it is also observed that the SPC treatment showed a mean Olsen-P concentration below that of the SNC treatment (Table 1). Phosphorous built-up concentrations in soil, when using SSs, is a point to be considered in the future, because in calcareous soils, P moves from the upper to the deeper soil layers, with a warning P concentration from 53 mg Olsen-P kg−1 [42]. In fact, a threshold of 80 mg P kg−1 has been established by the Catalan government (Spain) as a warning soil upper limit [39].

4.1. DTPA-Extractable Soil Elements

The critical levels of Fe, Zn, Cu and Mn found using the DTPA extraction method can vary between crops, but in different experiments described in [43], they were found to be close to 5, 1, 0.5, and 5 mg kg−1, respectively. These critical levels are surpassed in all treatments (Figure 1). However, the MIN treatment with 1.9 mg Zn kg−1 is approaching to the DTPA-Zn limit of 1.8 mg Zn kg−1 for soils with a pH of 8, which was established in a more detailed experiment by [44]. Zinc figures justify the introduction of sewage sludges to prevent potential Zn deficiencies.
Sewage sludge increased DTPA soil-extractable Cd, Cu and Zn and decreased Mn (Figure 1, Table A1), similar to the results obtained by [16] in calcareous soils. We disagree with [16] concerning the extractable Pb, as in our case, no differences were found between treatments (Figure 1, Table A1), although the maximum values were similar. The lack of Pb differences might be attributed to its adsorption onto the soil organic matter [8,45]. In SNC and SPC treatments, higher soil-extractable Cd, Cu, and Zn than in the MIN treatment were observed. In fact, Navarro et al. [6] stated that SSs increased Cd availability (although they applied much higher N rates (from 382 to 1328 kg N ha−1), and in our experiment, it was observed despite the expected absorption in carbonates forms) [46].
The increase in the DTPA extractability of Fe with SS treatments was followed by an inverse trend with extractable Mn. In iron, and in calcareous soils, extractable Fe is positively correlated with organic matter [47], and organic matter showed the highest values in the SPC and SNC treatments (Table 1). For the manganese, it has been described that its presence in SSs is highly bioavailable [5], but when applied, it is distributed and bound to carbonates [48]. Our data on extractable Mn (from 6 to 8 Mn kg−1, Figure 1) approach the average obtained by [47] (9 mg Mn kg−1) in calcareous soils. Also, data from [47] match Zn values for MIN, although our figures for SNC and SPC were close to their upper limit of 5.6 mg Zn kg−1. When comparing for iron, the SS treatments lead to available Fe concentrations above the maximum threshold of 12 mg Fe kg−1 from [47], which is advantageous for soils of high pH, where Fe availability is always a constraint [49].

4.2. Fractioned Plant Concentrations and Extractions

In the year of study, the described initial differences in extractable soil Cu and Zn nutrients (Figure 1, Table A6 and Table A7) did not translate into significant concentration differences in the grain, the cob and the biomass of the rest of the plant (Figure 3c,d). Thus, both extractable nutrients were neither limiting nor toxic. In fact, Zn concentrations (Figure 3c) were included in the acceptable levels of Zn in plant leaf tissues, which are from 10 to 100 mg kg−1 [50]. The upper Cu threshold in maize tissues was established in 20 mg Cu kg−1 [51], which is also a concentration higher than ours (Figure 3d).
Despite DTPA-Cd soil differences (Figure 1), Cd concentrations were low for all treatments, as they were in maize crops. Some authors consider maize to be a Cd hyperaccumulator, which means a shoot concentration of 0.01 g Cd in 100 g of plant dry matter [52]. Other authors [51] established in maize leaves a Cd critical interval of 5–20 mg kg−1. In our case, plant Cd concentrations were lower than 41 µg Cd kg−1 (Figure 3f); thus, they were far below the EU legislation for animal feed [13] and human food [14].
The opposite trend (DTPA-Fe vs. DTPA-Mn) was not maintained in maize-crop Fe and Mn concentrations. In maize grain, the Fe concentration increased in the SNC treatment, but the Mn concentration also increased in cobs for the SNC (always comparing with MIN, Figure 3c). The competence of both elements for root absorption has been well-known for a long time [53], but it was not observed in our experiment.
Iron concentrations in maize plants from 194 (SPC) to 244 (MIN) mg Fe kg−1 were higher than in the literature records [54]. Moreover, the Mn concentration in plants ranged from 191 (SPC) to 244 (MIN) mg Mn kg−1values that would be considered high (from 151–200 mg Mn kg−1) or even excessive (>200 Mn kg−1) if they were recorded in the ear leaf of maize [55]. Despite maize being considered an Fe-inefficient plant [56], our recorded Fe grain values were very high in all treatments (between 26–34 mg Fe kg−1), which doubled the figures (14.65 ± 1.85 mg Fe kg−1) of other authors [57]. However, we coincided with [57] in Zn grain concentrations (21–34 mg Zn kg−1 in our experiment, and 27.04 ± 2.76 mg Zn kg−1 in theirs).
In grain, the SNC treatment also presented the highest values of Cr (1.54 µg kg−1) with respect to MIN (0.51 µg kg−1) and SPC (0.32 µg kg−1) treatments. According to [58], an average concentration of 0.6 µg Cr kg−1 was found in corn (yellow) for human consumption in Greece. The obtained Cr concentrations did not imply a significantly higher Cr grain extraction in SNC vs. MIN (Figure 4c). Nevertheless, the highest concentration, similar to the one that can be found in different silages (from 1.0 to 2.2 µg Cr kg−1; [59]), is not limiting for animal feeding. Conversely, higher chromium intake (in form of trivalent chromium from maize grain) might positively affect biochemical parameters related to the carbohydrate and lipid metabolism in ruminants [60]. In humans, it has been argued that Cr contributes to normal macronutrient metabolism and the maintenance of normal blood glucose concentrations [61]. Fertilization with SSs and the related Cr concentration in grain is therefore an aspect that might be interesting to evaluate in the development of functional foods. However, the physiology of Cr accumulation in maize grain, when the SS highest rate is annually maintained for a long period, requires further research.
The average Co content in grain (c. 1.37 µg kg−1, Figure 3e) is lower than the concentration in a by-product of the manufacturing of maize starch (and sometimes ethanol) called maize gluten meal. This product is used for animal feed and usually has the highest concentration of Co (2 mg Co kg−1) of maize subproducts [62]. Thus, despite Co grain-concentration differences, all grains can be used for animal feed.
Concentration values from Pb and in all treatments (Figure 3e) are below the limits established by the EU for complete animal feed (5 mg Pb kg−1, 12% moisture [13]) and human consumption [14].
For macronutrients (N, P, K, Mg and S), sewage sludge treatments were only able to increase cob P concentration (vs. MIN), which might be interesting for animal feed when the entire cob is milled or just returned to the soil. For sulphur, concentrations in different parts of a maize plant varied from 0.7 to 0.8 g S kg−1 in cobs, 0.9 to 1.1 g S kg−1 in grain and 1.1 to 1.3 g S kg−1 in the rest of the plant. Around 1 g S kg−1 is the average value for maize fodder meal [60]. However, S availability requires further research as our concentrations were a bit lower that values recorded for mature plants [63,64].
In extractions, the significant differences found may affect future management strategies (Figure 4). Nitrogen extractions, from 200 kg N ha−1 (SPC) to 223 kg N ha−1 (MIN), alert us about potential N mining in the MIN treatment (Figure 4a) if organic matter is not replaced (Table 1). Moreover, it adds an advantage to the use of SS as a source of organic matter (Table 1) because of the additional available N when organic matter is mineralized. This is in addition to the other benefits to physical soil-quality properties found by [65].
From heavy metals, despite the higher soil-extractable Cd (Figure 2) in SS, cob Cd extraction was reduced in SS (Figure 4f). Mineral P fertilizers are also a Cd source (although concentrations vary according to the fertilizer origin [66]). The ordinary superphosphate is also a S source, and S can help in Cd mobility in calcareous soils [67], which might explain this contradictory behavior of higher Cd cob extraction in MIN.
For sulphur, the extraction of S in grain tended to decrease with SS. The uncertainty about S’s full availability might be related to the tendency toward high N concentration in grain in the MIN treatment. The N/S ratio in grain was 8.7, 11.3 and 11.7 for MIN, SPC and SNC, respectively. Sulphur favors N absorption [68]. Furthermore, sulphate uptake is also positively influenced by ammonium-N [64]. In the cited experiment [64], ammonium-N is applied in an MIN topdressing at a time of maximum S uptake, thus favoring both N and S uptake. Furthermore, in the MIN treatment, the ordinary mineral superphosphate (0-20-0-11S) is a source of sulphur as it has sulphates (mainly gypsum) in its formula [69]. Thus, in the MIN treatment, 55 kg S ha−1 is applied annually, which fully covers S demand (Figure 4b). In sludges, this interaction between nitrogen and sulphur might be limited, as N and S in SS are mainly in organic forms [70] and their plant availability requires mineralization.

5. Conclusions

The absence of yield differences between treatments supports the different fertilization strategies based on N criteria (mineral or SNC). The advantages of SS use (following N or P criteria) can be justified by the higher Cu, Fe and Zn soil availability, which is an agronomic advantage in calcareous soils. In the SNC, a higher Cr grain concentration than in the SPC can be also advantageous for animal feeding or/and in the development of new functional foods. However, from the environmental aspect, the SPC treatment appears as a sounder option to prevent available P becoming built up quickly, as well as for reducing cob Cd extractions (vs. MIN) using maize. In this highly productive maize system, the potential interaction of N vs. S in grain extractions requires further attention, as does the potential N mining effect in the MIN treatment.

Author Contributions

Conceptualization, F.C.-S., F.D.-O. and À.D.B.-S.; methodology, F.C.-S. and À.D.B.-S.; investigation, A.D.C.-A.; formal analysis, A.D.C.-A. and À.D.B.-S.; data curation, A.D.C.-A. and M.M.B.-B.; writing—original draft preparation, M.M.B.-B.; writing—review and editing, À.D.B.-S.; project administration, F.C.-S.; funding acquisition, F.C.-S. and F.D.-O. All authors have read and agreed to the published version of the manuscript.

Funding

Spanish Ministry of Economy and Competitiveness and the Spanish National Institute for Agricultural Research and Experimentation (MINECO-INIA) through the project RTA2017-88-C3-3. The experimental site maintenance was funded by IRTA-Mas Badia and the Department of Climate Action, Food and Rural Agenda from Generalitat de Catalunya, Catalonia, Spain.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available upon its reasonable request from the corresponding author.

Acknowledgments

The authors thank E. González for field support and M. Antúnez and S. Porras for their laboratory support.

Conflicts of Interest

The authors declare no conflicts of interest.

Appendix A

Table A1. Analysis of variance of extractable soil heavy metals with DTPA (μg kg−1) for fertilization treatments (FTs).
Table A1. Analysis of variance of extractable soil heavy metals with DTPA (μg kg−1) for fertilization treatments (FTs).
SourcedfFeCdCuMnPbZn
SSpSSpSSpSSpSSpSSp
FT2166,754,1620.00160.010.02719,971,891 0.00066,487,0790.000312990.7116,075,6430.0015
Block 363,827,4150.02022.330.2301,327,8460.232039,0400.849410,9670.21660,9110.0001
Error512,344,073-18.46-1,104,125-247,114-10,748-39,031-
Table A2. Analysis of variance for grain, cob and the rest of plant biomass (kg ha−1) for the fertilization treatments (FTs).
Table A2. Analysis of variance for grain, cob and the rest of plant biomass (kg ha−1) for the fertilization treatments (FTs).
SourcedfGrainCobPlant
SSpSSpSSp
FT233,685,8440.10686,3440.112,230,3550.65
Block37,652,4620.6879,8960.8522,793,8250.11
Error629,169,874-617,864-14,631,015-
Table A3. Analysis of variance of total N (%) and P (mg kg−1) in three parts of maize plants and for the fertilization treatments (FTs).
Table A3. Analysis of variance of total N (%) and P (mg kg−1) in three parts of maize plants and for the fertilization treatments (FTs).
SourcedfN (Grain)N (Cob)N (Plant)P (Grain)P (Cob)P (Plant)
SSpSSpSSpSSpSSpSSp
FT20.0110.560.0580.090.03780.51123,4280.60169,7110.011,850,6310.20
Block30.0070.850.0450.230.02020.84269,3180.5315,4680.662,450,4520.23
Error60.051-0.048-0.1479-665,227-54,989-2,602,463-
Table A4. Analysis of variance of K (mg kg−1) and Mg (mg kg−1) in three parts of maize plants and for the fertilization treatments (FTs).
Table A4. Analysis of variance of K (mg kg−1) and Mg (mg kg−1) in three parts of maize plants and for the fertilization treatments (FTs).
SourcedfK (Grain)K (Cob)K (Plant)Mg (Grain)Mg (Cob)Mg (Plant)
SSpSSpSSpSSpSSpSSp
FT267,1440.743,781,8610.50920,9030.8110,7700.88132,4050.12285,4450.42
Block 3364,9650.414,347,9020.6411,757,1360.2458,8250.7261,8960.47308,2510.57
Error6649,401-14,393,586-12,615,651-251,639-128,177-841,306-
Table A5. Analysis of variance of Fe (μg kg−1) and Mn (μg kg−1) in three parts of maize plants and for the fertilization treatments (FTs).
Table A5. Analysis of variance of Fe (μg kg−1) and Mn (μg kg−1) in three parts of maize plants and for the fertilization treatments (FTs).
SourcedfFe (Grain)Fe (Cob)Fe (Plant)Mn (Grain)Mn (Cob)Mn (Plant)
SSpSSpSSpSSpSSpSSp
FT2137,678,1350.0132,487,3620.696,143,637,8540.07845,8440.181,971,3210.03794,809,4400.25
Block 3122,150,3430.04119,603,9320.46609,140,2080.841,023,6230.231,003,6780.20242,565,5890.79
Error631,904,124-242,419,913-4,427,044,422-1,083,892-935,025-1,363,654,625-
Table A6. Analysis of variance of S (mg kg−1) and Cu (μg kg−1) in three parts of maize plants and for the fertilization treatments (FTs).
Table A6. Analysis of variance of S (mg kg−1) and Cu (μg kg−1) in three parts of maize plants and for the fertilization treatments (FTs).
SourcedfS (Grain)S (Cob)S (Plant)Cu (Grain)Cu (Cob)Cu (Plant)
SSpSSpSSpSSpSSpSSp
FT2104,3480.2323,9810.7557,0290.27108,4960.52106,5710.592,906,1220.19
Block 337,3080.7349,2000.7565,7480.37118,8480.67663,1690.16967,5430.70
Error6165,273-237,930-105,677-440,236-548,684-3,911,138-
Table A7. Analysis of variance of Zn (μg kg−1) in three parts of maize plants and for the fertilization treatments (FTs).
Table A7. Analysis of variance of Zn (μg kg−1) in three parts of maize plants and for the fertilization treatments (FTs).
SourcedfZn (Grain)Zn (Cob)Zn (Plant)
SSpSSpSSp
FT216,527,9720.53454,364,4350.16324,683,8320.08
Block 315,949,4740.73154,910,2760.65119,972,4120.44
Error670,675,662-541,500,685-188,169,463-
Table A8. Analysis of variance of Cd (μg kg−1) and Co (μg kg−1) in three parts of maize plants and for the fertilization treatments (FTs).
Table A8. Analysis of variance of Cd (μg kg−1) and Co (μg kg−1) in three parts of maize plants and for the fertilization treatments (FTs).
SourcedfCd (Grain)Cd (Cob)Cd (Plant)Co (Grain)Co (Cob)Co (Plant)
SSpSSpSSpSSpSSpSSp
FT20.500.534.660.172400.076280.05320.8011990.03
Block 30.120.951.090.78760.493380.25900.731550.65
Error62.13-5.83-166-375-411-541-
Table A9. Analysis of variance of Cr (μg kg−1) and Pb (μg kg−1) in three parts of maize plants and for the fertilization treatments (FTs).
Table A9. Analysis of variance of Cr (μg kg−1) and Pb (μg kg−1) in three parts of maize plants and for the fertilization treatments (FTs).
SourcedfCr (Grain)Cr (Cob)Cr (Plant)Pb (Grain)Pb (Cob)Pb (Plant)
SSpSSpSSpSSpSSpSSp
FT23,407,0170.016269,6580.88132,9990.045670.488.90.9587830.003
Block 3751,5880.3541,445,8690.71130,8560.092240.28389.50.3318000.151
Error6114,5954-6,109,310-73,775-108-438.6-1406-
Table A10. Analysis of variance of N (kg ha−1) and P (kg ha−1) in three parts of maize plants and for the fertilization treatments (FTs).
Table A10. Analysis of variance of N (kg ha−1) and P (kg ha−1) in three parts of maize plants and for the fertilization treatments (FTs).
SourcedfN (Grain)N (Cob)N (Plant)P (Grain)P (Cob)P (Plant)
SSpSSpSSpSSpSSpSSp
FT227980.03616.70.3868.00.9019.30.630.400.08271.60.07
Block 374150.008137.10.03638.00.605220.010.990.03146.40.31
Error61375-43.5-1923.7-116-0.31-194.9-
Table A11. Analysis of variance of K (kg ha−1) and Mg (kg ha−1) in three parts of maize plants and for the fertilization treatments (FTs).
Table A11. Analysis of variance of K (kg ha−1) and Mg (kg ha−1) in three parts of maize plants and for the fertilization treatments (FTs).
SourcedfK (Grain)K (Cob)K (Plant)Mg (Grain)Mg (Cob)Mg (Plant)
SSpSSpSSpSSpSSpSSp
FT21510.337.30.822014.30.319.90.2970.250.3839.20.40
Block 310960.0392.50.272014.10.47112.30.0070.100.8214.30.85
Error6340-109.0-4206.4-19.9-0.65-108.8-
Table A12. Analysis of variance of S (kg ha−1) and Cu (g ha−1) in three parts of maize plants and for the fertilization treatments (FTs).
Table A12. Analysis of variance of S (kg ha−1) and Cu (g ha−1) in three parts of maize plants and for the fertilization treatments (FTs).
SourcedfS (Grain)S (Cob)S (Plant)Cu (Grain)Cu (Cob)Cu (Plant)
SSpSSpSSpSSpSSpSSp
FT253.50.050.270.5818.80.11204.10.124.90.1880.20.86
Block 324.80.300.610.499.90.40433.10.0623.20.02547.30.59
Error632.7-1.36-16.9-198.5-6.5-1568.3-
Table A13. Analysis of variance of Fe (g ha−1) and Mn (kg ha−1) in three parts of maize plants and for the fertilization treatments (FTs).
Table A13. Analysis of variance of Fe (g ha−1) and Mn (kg ha−1) in three parts of maize plants and for the fertilization treatments (FTs).
SourcedfFe (Grain)Fe (Cob)Fe (Plant)Mn (Grain)Mn (Cob)Mn (Plant)
SSpSSpSSpSSpSSpSSp
FT212,1410.17697.60.32217,6870.550.000064700.5830.000000860.6780.0620.35
Block 344,9100.042437.80.10167,8880.800.002190730.0050.000034110.0080.0370.69
Error611,979-1522.6-1,000,876-0.00032780-0.00000621-0.147-
Table A14. Analysis of variance of Zn (g ha−1) in 3 parts of maize and for the fertilization treatments.
Table A14. Analysis of variance of Zn (g ha−1) in 3 parts of maize and for the fertilization treatments.
SourcedfZn (Grain)Zn (Cob)Zn (Plant)
SSpSSpSSp
Treatments27290.829860.4152,518.960.08
Block 331,3610.034150.8316,797.760.49
Error611,025-2867-30,398.92-
Table A15. Analysis of variance of Cd (mg ha−1) and Co (mg ha−1 for grain and plant; μg ha−1 for cob) in maize and for the fertilization treatments (FTs).
Table A15. Analysis of variance of Cd (mg ha−1) and Co (mg ha−1 for grain and plant; μg ha−1 for cob) in maize and for the fertilization treatments (FTs).
SourcedfCd (Grain)Cd (Cob)Cd (Plant)Co (Grain)Co (Cob)Co (Plant)
SSpSSpSSpSSpSSpSSp
FT21470.5549.70.0478340.631420.16233,305,9910.6666.50.18
Block 32060.6331.10.1877520.811240.312,201,358,8970.1379.90.24
Error6672-27.3-47,660-169-1,554,154,077-87.1-
Table A16. Analysis of variance of Cr (g ha−1) and Pb (mg ha−1) in three parts of maize plants and for the fertilization treatments (FTs).
Table A16. Analysis of variance of Cr (g ha−1) and Pb (mg ha−1) in three parts of maize plants and for the fertilization treatments (FTs).
SourcedfCr (Grain)Cr (Cob)Cr (Plant)Pb (Grain)Pb (Cob)Pb (Plant)
SSpSSpSSpSSpSSpSSp
FT2734.50.0495.470.543.40.6681880.5432.00.97625,8750.41
Block 3351.90.27527.540.184.60.7546,2960.204438.20.151,191,4360.36
Error6426.1-24.03-22.6-16,027-2720.1-1,837,439-

References

  1. European Comission. Proposal for a Directive of the European Parliament and of the Council Concerning Urban Wastewater Treatment (Recast). Available online: https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX%3A52022PC0541&qid=1668778087100 (accessed on 5 August 2024).
  2. Directive 2008/98/EC of the European Parliament and of the Council of 19 November 2008 on Waste and Repealing Certain Directives. Available online: http://data.europa.eu/eli/dir/2008/98/2024-02-18 (accessed on 5 August 2024).
  3. Ministerio de Medio Ambiente y Medio Rural y Marino. Caracterización de los Lodos de Depuradoras Generados en España; MARM: Madrid, Spain, 2009; Available online: https://www.miteco.gob.es/es/calidad-y-evaluacion-ambiental/publicaciones/lodos.html (accessed on 5 August 2024).
  4. Lodos de Depuración de Aguas Residuales. Available online: https://www.miteco.gob.es/en/calidad-y-evaluacion-ambiental/temas/prevencion-y-gestion-residuos/flujos/lodos-depuradora.html (accessed on 5 August 2024).
  5. Nkinahamira, F.; Suanon, F.; Chi, Q.; Li, Y.; Feng, M.; Huang, X.; Yu, C.-P.; Sun, Q. Occurrence, geochemical fractionation, and enviornmental risk assessment of major and trace elements in sewage sludge. J. Environ. Manag. 2019, 249, 109427. [Google Scholar] [CrossRef] [PubMed]
  6. Navarro-Pedreño, J.; Almendro-Candel, M.B.; Jordán-Vidal, M.M.; Mataix-Solera, J.; García-Sánchez, E. Mobility of cadmium, chromium, and nickel through the profile of a calcisol treated with sewage sludge in the southeast of Spain. Environ. Earth Sci. 2003, 44, 545–553. [Google Scholar] [CrossRef]
  7. Pascual, I.; Antolín, M.C.; García, C.; Polo, A.; Sánchez-Díaz, M. Plant availability of heavy metals in a soil amended with a high dose of sewage sludge under drought conditions. Biol. Fertil. Soil 2004, 40, 291–299. [Google Scholar] [CrossRef]
  8. Morera, M.Y.; Echevarría, J.C.; Garrido, J.J. Mobility of heavy metals in soils amended with sewage sludge. Can. J. Soil Sci. 2011, 81, 405–414. [Google Scholar] [CrossRef]
  9. Wierzbowska, J.; Sienkiewicz, S.; Załuski, D. Nitrogen fractions in soil fertilized with waste organic materials. Agronomy 2021, 11, 1474. [Google Scholar] [CrossRef]
  10. Nepal, A.; Antonious, G.F.; Bebe, F.N.; Webster, T.C.; Gyawali, B.R.; Neupane, B. Heavy metal accumulation in three varieties of mustard grown under five soil management practices. Environments 2024, 11, 77. [Google Scholar] [CrossRef]
  11. Hamdia, H.; Hechmia, S.; Khelilb, M.N.; Zoghlamia, I.R.; Benzartic, S.; Mokni-Tlilia, S.; Hassena, A.; Jedidia, N. Repetitive land application of urban sewage sludge: Effect of amendment rates and soil texture on fertility and degradation parameters. Catena 2018, 172, 11–20. [Google Scholar] [CrossRef]
  12. Arrobas, M.; Meneses, R.; Gusmão, A.G.; da Silva, J.M.; Correia, C.M.; Rodrigues, M.Â. Nitrogen-Rich Sewage Sludge Mineralized Quickly, Improving Lettuce Nutrition and Yield, with Reduced Risk of Heavy Metal Contamination of Soil and Plant Tissues. Agronomy 2024, 14, 924. [Google Scholar] [CrossRef]
  13. Rodrigues, M.Â.; Sawimbo, A.; da Silva, J.M.; Correia, C.M.; Arrobas, M. Sewage sludge increased lettuce yields by releasing valuable nutrients while keeping heavy metals in soil and plants at levels well below international legislative limits. Horticulturae 2024, 10, 706. [Google Scholar] [CrossRef]
  14. Namdari, M.; Soleimani, M.; Mirghaffari, N.; Kharrazi, S.M. Effect of biological sewage sludge and its derived biochar on accumulation of potentially toxic elements by corn (Zea mays L.). Sci. Rep. 2024, 14, 5985. [Google Scholar] [CrossRef]
  15. Demitrelos, E.; Koukoulakis, P.H.; Kyritsis, S.S.; Bountla, A.; Isari, E.; Kalavrouziotis, I.K. Impact of elemental interactions on soil metal availability and growth of ryegrass (Lolium perenne L.) under wastewater and biosolids. Water Air Soil Pollut. 2022, 233, 96. [Google Scholar] [CrossRef]
  16. Zaragüeta, A.; Enrique, A.; Virto, I.; Antón, R.; Urmeneta, H.; Orcaray, L. Effect of the long-term application of sewage sludge to a calcareous soil on its total and bioavailable content in trace elements, and their transfer to the crop. Minerals 2021, 11, 356. [Google Scholar] [CrossRef]
  17. Iglesias, M.; Marguí, E.; Camps, F.; Hidalgo, M. Extractability and crop transfer of potentially toxic elements from mediterranean agricultural soils following long-term sewage sludge applications as a fertilizer replacement to barley and maize crops. J. Waste Manag. 2018, 75, 312–318. [Google Scholar] [CrossRef]
  18. Kanengoni, A.T.; Chimonyo, M.; Ndimba, B.K.; Dzama, K. Potential of using maize cobs in pig diets—A review. Asian Australas. J. Anim. Sci. 2015, 28, 1669–1679. [Google Scholar] [CrossRef]
  19. Real Decreto 1310/1990, de 29 de Octubre, por el que se Regula la Utilización de los Lodos de Depuración en el Sector Agrario. Available online: https://www.boe.es/eli/es/rd/1990/10/29/1310/con (accessed on 5 August 2024).
  20. Real Decreto 1051/2022, de 27 de Diciembre, por el que se Establecen Normas para la Nutrición Sostenible en los Suelos Agrarios. Available online: https://www.boe.es/eli/es/rd/2022/12/27/1051 (accessed on 5 August 2024).
  21. Directive 2002/32/EC of the European Parliament and of the Council of 7 May 2002 on Undesirable Substances in Animal Feed. Available online: http://data.europa.eu/eli/dir/2002/32/2019-11-28 (accessed on 5 August 2024).
  22. Commission Regulation (EU) 2023/915 of 25 April 2023 on Maximum Levels for Certain Contaminants in Food and Repealing Regulation (EC) No 1881/2006. Available online: http://data.europa.eu/eli/reg/2023/915/2024-04-25 (accessed on 5 August 2024).
  23. UNE 77322:2003; Soil Quality. Extraction of Trace Elements Soluble in Agua Regia. Available online: https://www.une.org/encuentra-tu-norma/busca-tu-norma/norma/?c=N0028932 (accessed on 5 August 2024).
  24. Feng, M.-H.; Shan, X.-Q.; Zhang, S.; Wen, B. A comparison of the rhizosphere-based method with DTPA, EDTA, CaCl2, and NaNO3 extraction methods for prediction of bioavailability of metals in soil to barley. Environ. Pollut. 2005, 137, 231–240. [Google Scholar] [CrossRef]
  25. DECRET 136/2009, d’1 de Setembre, d’Aprovació del Programa d’Actuació Aplicable a les Zones Vulnerables en Relació amb la Contaminació de Nitrats que Procedeixen de Fonts Agràries i de Gestió de les Dejeccions Ramaderes. Available online: https://portaljuridic.gencat.cat/eli/es-ct/d/2009/09/01/136 (accessed on 5 August 2024).
  26. Soil Survey Staff. Keys to Soil Taxonomy, 13th ed.; USDA-Natural Resources Conservation Services: Washington, DC, USA, 2022. [Google Scholar]
  27. Camps-Sagué, F. (IRTA Mas Badia, Agricultural Experimental Station Mas Badia, La Tallada d’Empordà, Girona, Spain). Personal communication, 2024. [Google Scholar]
  28. Walkley, A.; Black, I.A. An examination of the Degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Sci. 1934, 37, 29–38. [Google Scholar] [CrossRef]
  29. Pansu, M.; Gautheyrou, J. Chapter 29: Phosphorus. In Handbook of Soil Analysis. Mineralogical, Organic and Inorganic Methods; Pansu, M., Gautheyrou, J., Eds.; Springe: Dordrecht, The Netherlands, 2003; p. 809. [Google Scholar]
  30. Hendershot, W.H.; Lalande, H.; Duquette, M. Ion exchange and exchangeable cations. In Soil Sampling and Methods of Analysis, 2nd ed.; Carter, M.R., Gregorich, E.G., Eds.; Canadian Society of Soil Science, CRC Press and Taylor and Francis Group: Boca Raton, FL, USA, 2008; pp. 197–206. [Google Scholar]
  31. UNE.EN 16174; Sludge, Treated Biowaste and Soil—Digestion of Aqua Regia Soluble Fractions of Elements. Asociación Española de Normalización y Certificación: Madrid, España, 2012.
  32. Baker, D.E.; Amacher, M.C. Nickel, copper, zinc and cadmium. In Methods of Soil Analysis, Part 2, Chemical and Microbiological Properties, 2nd ed.; Page, A.L., Ed.; ASA, SSSA: Madison, WI, USA, 1982; pp. 323–336. [Google Scholar]
  33. González, D.; Almendros, P.; Álvarez, J.M. Métodos de análisis de elementos en suelos: Disponibilidad y fraccionamiento. An. Quím. RSEQ 2009, 105, 205–212. [Google Scholar]
  34. UNE-EN 16171; Sludge, Treated Biowaste and Soil—Determination of Elements Using Inductively Coupled Plasma Mass Spectrometry (ICP-MS). Asociación Española de Normalización y Certificación: Madrid, España, 2012.
  35. McGill, W.B.; Figuereido, C.T. Chapter 22: Total Nitrogen. In Soil Sampling and Method of Analysis; Carter, M., Ed.; CRC Press: Boca Raton, FL, USA, 1993; pp. 201–207. [Google Scholar]
  36. UNE-EN 15621; Alimentos para Animales. Métodos de Muestreo y Análisis. Determinación del Calcio, Sodio, Fósforo, Magnesio, Potasio, Azufre, Hierro, Zinc, Cobre, Manganeso y Cobalto tras Digestión bajo Presión mediante ICP-AES. Asociación Española de Normalización y Certificación: Madrid, España, 2018.
  37. UNE-EN ISO 6869:2001; Alimentos para Animales. Determinación del Contenido de Calcio, Cobre, Hierro, Magnesio, Manganeso, Potasio, Sodio y Zinc. Método por Espectrometría de Absorción Atómica. Asociación Española de Normalización y Certificación: Madrid, España, 2001.
  38. SAS Institute Inc. SAS/TAT; Software V 9.4; SAS Institute: Cary, NC, USA, 2002. [Google Scholar]
  39. Decree 153/2019, of 3rd July, on the Management of Soil Fertilization and Manure, and the Implementation of the Action Program in Vulnerable Areas in Relation to Nitrate Pollution from Agricultural Sources. Available online: https://portaljuridic.gencat.cat/eli/es-ct/d/2019/07/03/153 (accessed on 26 August 2024).
  40. Epstein, E. Land Application of Sewage Sludge and Biosolids, 1st ed.; CRC Press: Boca Raton, FL, USA, 2002. [Google Scholar]
  41. Shakoor, A.; Bosch-Serra, À.D.; Olarieta Alberdi, J.R.; Herrero, C. Seven years of pig slurry fertilization: Impacts on soil chemical properties and the element content of winter barley plants. Environ. Sci. Pollut. Res. 2022, 29, 74655–74668. [Google Scholar] [CrossRef]
  42. Ortiz, C.; Pierotti, S.; Molina, M.G.; Bosch-Serra, À.D. Soil fertility and phosphorus leaching in irrigated calcareous soils of the mediterranean region. Environ. Monit. Assess. 2023, 195, 1376. [Google Scholar] [CrossRef] [PubMed]
  43. Martens, D.C.; Lindsay, W.L. Testing soils for copper, iron, manganese, and zinc. In Soil Testing and PLANT analysis, 3rd ed.; Westermann, R.L., Ed.; SSSA: Madison, WI, USA, 1990; pp. 229–264. [Google Scholar]
  44. Loué, A. Les Oligo-Éléments en Agriculture, 7th ed.; Agri-Nathan International: Paris, France, 1986. [Google Scholar]
  45. Gu, X.; Sun, J.; Evans, L.J. The development of a multi-surface soil speciation model for Cd (II) and Pb (II): Comparison of two approaches for metal adsorption to clay fractions. Appl. Geochem. 2014, 47, 99–108. [Google Scholar] [CrossRef]
  46. Pardo, F.; Jordán, M.M.; Sanfeliu, T.; Pina, S. Distribution of Cd, Ni, Cr, and Pb in amended soils from Alicante province (SE, Spain). Water Air Soil Pollut. 2011, 217, 535–543. [Google Scholar] [CrossRef]
  47. Abadía, J.; Millán, E.; Montañés, L.; García, L. DTPA and NH4 HCO3-DTPA extractable Fe, Mn and Zn levels in the Ebro Valley. An. Estac. Exp. 1980, 15, 181–193. Available online: https://digital.csic.es/bitstream/10261/22044/1/ANALES15-1-2Abad%c3%adaJ%2cMill%c3%a1nL.pdf (accessed on 5 August 2024).
  48. Moral, R.; Gilkes, R.J.; Jordán, M.M. Distribution of heavy metals in calcareous and non-calcareous soils in Spain. Water Air Soil Pollut. 2005, 162, 127–142. [Google Scholar] [CrossRef]
  49. Sánchez Alcalá, I. Bioavailability of Iron in Calcareous Soils: Microbial Reduction and Nanofertilizer Application. Ph.D. Thesis, Universidad de Córdoba, Córdoba, Spain, 2012. [Google Scholar]
  50. Jones, J.B. Plant Nutrition and Soil Fertility Manual: How to Make Soil Fertility Plant Nutrition Principles Work, 2nd ed.; CRC Press: Boca Raton, FL, USA, 2012. [Google Scholar]
  51. Macnicol, R.D.; Beckett, P.H.T. Critical tissue concentrations of potentially toxic elements. Plant Soil 1985, 85, 107–129. [Google Scholar] [CrossRef]
  52. Ling, T.; Gao, Q.; Dua, H.; Zhao, Q.; Ren, J. Growing, physiological responses and Cd uptake of corn (Zea mays L.) under different Cd supply. Chem. Spec. Bioavailab. 2017, 29, 216–221. [Google Scholar] [CrossRef]
  53. Shim, S.C.; Vose, P.B. Varietal differences in the kinetics of iron uptake by excised roots. J. Exp. Bot. 1965, 16, 216–232. [Google Scholar] [CrossRef]
  54. Aref, F. Manganese, iron and copper contents in leaves of maize plants (Zea mays L.) grown with different boron and zinc micronutrients. Afr. J. Biotechnol. 2012, 11, 896–903. [Google Scholar] [CrossRef]
  55. Reuter, D.J.; Robinson, J.B. Plant Analysis: An Interpretation Manual, 2nd ed.; CSIRO: Collingwood, ON, USA, 1997. [Google Scholar]
  56. Keigler, J.I.; Wiesinger, J.A.; Flint-Garcia, S.A.; Glahn, R.P. Iron bioavailability of maize (Zea mays L.) after removing the germ fraction. Front. Plant Sci. 2023, 14, 1114760. [Google Scholar] [CrossRef]
  57. Hindu, V.; Palacios-Rojas, N.; Babu, R.; Suwarno, W.B.; Zerka, R.; Usha, R.; Saykhedkar, G.R.; Nair, S.K. Identificaction and validaton of genomic regions influencing kernel zinc and iron in maize. Theor. Appl. Genet. 2018, 131, 1443–1457. [Google Scholar] [CrossRef]
  58. Bratakos, M.S.; Lazos, E.S.; Bratakos, S.M. Chromium content of selected Greek foods. Sci. Total Environ. 2002, 290, 47–58. [Google Scholar] [CrossRef]
  59. Bryan, M.A.; Socha, M.T.; Tomlinson, D.J. Supplementing intensively grazed late-gestation and early lactation dairy cattle with chromium. J. Dairy. Sci. 2004, 87, 4269–4277. [Google Scholar] [CrossRef] [PubMed]
  60. Lashkari, S.; Habibian, M.; Jensen, S.K. A review on the role of chromium supplementation in rumiant nutrition-effects on productive performance, blood metabolite, antioxidant status, and immunocompetence. Biol. Trace Elem. Res. 2018, 186, 305–321. [Google Scholar] [CrossRef]
  61. European Food Safety Authority (EFSA). Scientific Opinion on the substantiation of health claims related to chromium and contribution to normal macronutrient metabolism (ID 260, 401, 4665, 4666, 4667), maintenance of normal blood glucose concentrations (ID 262, 4667), contribution to the maintenance or achievement of a normal body weight (ID 339, 4665, 4666), and reduction of tiredness and fatigue (ID 261) pursuant to Article 13(1) of Regulation (EC) No 1924/2006. EFSA J. 2010, 8, 1723–1746. [Google Scholar] [CrossRef]
  62. Sauvant, D.; Pérez, J.M.; Tran, G. Tablas de Composición y de Valor Nutritivo de las Materias Primas Destinadas a los Animales de Interés Ganadero, 1st ed.; Mundiprensa: Madrid, Spain, 2004. [Google Scholar]
  63. Degryse, F.; Baird, R.; da Silva, R.C.; Holzapfel, C.B.; Kappes, C.; Tysko, M.; McLaughlin, M.J. Sulfur uptake from fertilizer fortified with sulfate and elemental S in three contrasting climatic zones. Agronomy 2020, 10, 1035. [Google Scholar] [CrossRef]
  64. Barber, S.A. Soil Nutrient Bioavailability: A Mechanistic Approach, 2nd ed.; Wiley and Sons: Hoboken, NJ, USA, 1995; pp. 301–310. [Google Scholar]
  65. Camps-Sagué, F.; Lavaquiol, B.; Bosch-Serra, À.D.; Molina, M.G.; Domingo-Olivé, F. Sustainability assessment after twenty years of sewage sludge application on calcareous soil following N or P criterion. Sustainability 2024, 16, 2304. [Google Scholar] [CrossRef]
  66. Mortvedt, J.J. Heavy Metals in Fertilisers: Their ffect on Soil and Plant Health. In Proceedings of the No: 575. The International Fertiliser Society, Cambridge, UK, 8 December 2005. [Google Scholar]
  67. Kayser, A.; Wenger, K.; Keller, A.; Attinger, W.; Felix, H.R.; Gupta, S.K.; Schulin, R. Enhancement of phytoextraction of Zn, Cd, and Cu from calcareous soil: The use of NTA and sulfur amendments. Environ. Sci. Technol. 2000, 34, 1778–1783. [Google Scholar] [CrossRef]
  68. Brodowska, M.S.; Wyszkowski, M.; Karsznia, M. Application of urea and ammonium nitrate solution with potassium thiosulfate as a factor determining macroelement contents in plants. Agronomy 2024, 14, 1097. [Google Scholar] [CrossRef]
  69. Barker, A.V. Fertilizers. In Encyclopedia of Analytical Science, 3rd ed.; Worsfold, P., Poole, C., Townshend, A., Miró, M., Eds.; Elsevier: Amsterdam, The Netherlands, 2019; pp. 134–144. [Google Scholar] [CrossRef]
  70. Sommers, L.E.; Tabatabai, M.A.; Nelson, D.W. Forms of sulfur in sewage sludge. J. Environ. Qual. 1977, 6, 42–46. [Google Scholar] [CrossRef]
Applsci 14 08105 g001
Figure 1. Average values of soil available Cd (mg 102 Cd kg−1) and available Cu, Fe, Mn, Pb, and Zn (mg kg−1) in soil, determined by DTPA extraction, for each fertilization strategy (MIN: mineral; SPC: sewage sludge, P criterion; SNC: sewage sludge, N criterion). For each element, means with different letters are significantly different according to the Duncan’s multiple-range test (α = 0.05).
Figure 1. Average values of soil available Cd (mg 102 Cd kg−1) and available Cu, Fe, Mn, Pb, and Zn (mg kg−1) in soil, determined by DTPA extraction, for each fertilization strategy (MIN: mineral; SPC: sewage sludge, P criterion; SNC: sewage sludge, N criterion). For each element, means with different letters are significantly different according to the Duncan’s multiple-range test (α = 0.05).
Applsci 14 08105 g001
Applsci 14 08105 g002
Figure 2. Accumulated dry-matter yield (Mg ha−1) from different parts of maize plants and for each treatment (MIN: mineral; SPC: sewage sludge, P criterion; SNC: sewage sludge, N criterion). No significant differences were found between fertilization treatments in dry-matter yields.
Figure 2. Accumulated dry-matter yield (Mg ha−1) from different parts of maize plants and for each treatment (MIN: mineral; SPC: sewage sludge, P criterion; SNC: sewage sludge, N criterion). No significant differences were found between fertilization treatments in dry-matter yields.
Applsci 14 08105 g002
Applsci 14 08105 g003
Figure 3. Average concentrations of N and K (a); P, Mg and S (b); Fe, Mn and Zn (c); Cr and Cu (d); Co and Pb (e); and Cd (f); in different parts of maize plants for each treatment (MIN: mineral; SPC: sewage sludges, P criterion; SNC: sewage sludges, N criterion). In grain, for Co, Cr and Fe; in cob, for P and Mn; and Co, Cr and Pb in plant; means with different letters are significantly different according to the DMRT (α = 0.05).
Figure 3. Average concentrations of N and K (a); P, Mg and S (b); Fe, Mn and Zn (c); Cr and Cu (d); Co and Pb (e); and Cd (f); in different parts of maize plants for each treatment (MIN: mineral; SPC: sewage sludges, P criterion; SNC: sewage sludges, N criterion). In grain, for Co, Cr and Fe; in cob, for P and Mn; and Co, Cr and Pb in plant; means with different letters are significantly different according to the DMRT (α = 0.05).
Applsci 14 08105 g003
Applsci 14 08105 g004
Figure 4. Accumulated average extractions of N and K (a); P, Mg and S (b); Cr, Cu and Mn (c); Co and Pb (d); Fe and Zn (e); and Cd (f); from average extractions in different parts of maize plants, and for each treatment (MIN: mineral; SPC: sewage sludges, P criterion; SNC: sewage sludges, N criterion). In grain, for Cr, N and S; in cob, for Cd; and in straw, for P and Zn; means with different letters are significantly different according to the DMRT (α = 0.05).
Figure 4. Accumulated average extractions of N and K (a); P, Mg and S (b); Cr, Cu and Mn (c); Co and Pb (d); Fe and Zn (e); and Cd (f); from average extractions in different parts of maize plants, and for each treatment (MIN: mineral; SPC: sewage sludges, P criterion; SNC: sewage sludges, N criterion). In grain, for Cr, N and S; in cob, for Cd; and in straw, for P and Zn; means with different letters are significantly different according to the DMRT (α = 0.05).
Applsci 14 08105 g004
Table 1. Soil physicochemical parameters 1 of the upper layer (0–0.2 m) in October 2018 sampling, and from the different treatments: mineral (MIN), sludge N criterion (SNC), sludge P criterion (P). Parameter results from the sewage sludge (SS) applied in March 2019 are also included.
Table 1. Soil physicochemical parameters 1 of the upper layer (0–0.2 m) in October 2018 sampling, and from the different treatments: mineral (MIN), sludge N criterion (SNC), sludge P criterion (P). Parameter results from the sewage sludge (SS) applied in March 2019 are also included.
SourceOxidizable-OMOlsen-PK (NH4OAc)Total-CdTotal-CuTotal-CrTotal-PbTotal-Zn
(g kg−1)(mg kg−1)
MIN-Soil1214.999<0.544.31817.872.2
SPC-Soil1539.296<0.552.419.518.682.2
SNC-Soil1657.187<0.552.517.419.182.8
Sludge69.219.53.041.1666838681208
1 All results are expressed over dry-matter basis.
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Camps-Sagué, F.; Bosch-Serra, À.D.; Cifuentes-Almeida, A.D.; Boixadera-Bosch, M.M.; Domingo-Olivé, F. Long-Term Amendment with Sewage Sludge: Effects on Nutrient Value and Trace-Metal Content in Different Parts of Maize Plants. Appl. Sci. 2024, 14, 8105. https://doi.org/10.3390/app14188105

AMA Style

Camps-Sagué F, Bosch-Serra ÀD, Cifuentes-Almeida AD, Boixadera-Bosch MM, Domingo-Olivé F. Long-Term Amendment with Sewage Sludge: Effects on Nutrient Value and Trace-Metal Content in Different Parts of Maize Plants. Applied Sciences. 2024; 14(18):8105. https://doi.org/10.3390/app14188105

Chicago/Turabian Style

Camps-Sagué, Francesc, Àngela Dolores Bosch-Serra, Alicia Daniela Cifuentes-Almeida, Montserrat Maria Boixadera-Bosch, and Francesc Domingo-Olivé. 2024. "Long-Term Amendment with Sewage Sludge: Effects on Nutrient Value and Trace-Metal Content in Different Parts of Maize Plants" Applied Sciences 14, no. 18: 8105. https://doi.org/10.3390/app14188105

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop