Can sewage sludge increase soil fertility and replace inorganic fertilizers for pineapple production?

Sewage sludge from treatment plants is an important source of N and organic matter for agriculture. The objective of this study was to analyze the effect of sewage sludge and mineral fertilization on the soil chemical properties and production of five pineapple cultivars. The study was conducted in 2 x 5 factorial scheme, consisting of two different fertilizers (sewage sludge and mineral fertilizers), combined with five pineapple cultivars (‘Pérola’, ‘Vitória’, ‘Smooth Cayenne’, ‘MD-2’, and ‘IAC Fantástico’). Sewage sludge fertilization favoured soil fertility by promoting a decrease in the pH and increase in the content of soil organic matter, phosphorus, calcium, iron, and zinc, compared to soil with mineral fertilization. In pineapple plants, sewage sludge fertilization provided statistically similar yields and physic chemical fruit characteristics compared to mineral fertilization. Among cultivars, the ‘Smooth Cayenne’ presented the highest yield (125 t ha), followed by cultivars ‘MD-2’ and ‘IAC Fantástico’, with intermediate yields of 98 and 90 t ha. Cultivars ‘Pérola’ and ‘Vitória’ presented lower yields. In this context, it was observed that sewage sludge can be used in pineapple cultivars, as an alternative source of nutrients to partial replaces inorganic fertilization.


Introduction
Sewage sludge is a material abundant in organic matter and essential elements to plants that can be used in agriculture (Berton & Nogueira, 2010;Nicolás et al., 2014;Qayyum et al., 2015;Li et al., 2020;Rehman & Qayyum, 2020). Considering the importance of this crop to Brazil and regions with semiarid climate, the use of sewage sludge in pineapple farming may contribute to a reduction in the use of mineral fertilizers, increase soil fertility and the production of pineapple cultivars.
Soils located in regions of tropical climate are poor in nitrogen, phosphorus, and exchangeable bases, and agronomic practices are required in order to improve their chemical conditions for the planting of species of economic interest. In this sense, the application of sewage sludge has increased soil fertility and productivity in various crops, such as corn, barley, sugarcane, rice, and wheat (Latare et al., 2014;Nascimento et al., 2015;McCray et al., 2017;Bastida et al., 2019;Mohamed et al., 2019).
The use of sewage sludge in agricultural promotes the plant nutrition through the greater availability of N (Latare et al., 2014;Ociepa et al., 2017;Melo et al., 2018;Mohamed et al., 2019), a corrective effect of soil acidity, in addition to providing other nutrients for plants. According to Bittencourt et al. (2017), the sludge applied to agricultural areas in the state of Paraná provided 90% of limestone (PRNT 75%), 69% of nitrogen, 83% of P2O5 and 35% of the K2O demanded by agricultural and forestry crops.
However, for pineapple crops, the use of sludge as a source of nutrients can alter the fruit production and quality intended for the juice production industry or in natura consumption, requiring new scientific information. The objective of this study was to evaluate the effects of sewage sludge and mineral fertilization on the soil chemical properties and production attributes of five pineapple cultivars.

Methodology
The study was conducted in the experimental area of the Sewage Treatment Plant (ETE) of the Minas Gerais Sanitation Company (COPASA), in Janaúba-MG, located at 15º 43 '47.4 "S and 43º 19' 22.1" W, with an elevation of 516 m.

The soil of the experimental area is as a Latossolo Vermelho eutrófíco according to the Brazilian Soil Classification
System (Santos et al., 2018a). The treatments were arranged in a randomized block design with four replications, in a 2 x 5 factorial scheme, consisting of two different fertilizers -sewage sludge (SS) and mineral fertilization (MF) -and five pineapple cultivars ('Pérola','Vitória','Smooth Cayenne',and'IAC Fantástico').
At planting, the pineapples received 3 g per plant of P2O5 in the form of single superphosphate (Cardoso et al., 2013).
To evaluate possible changes in the soil chemical attributes, after fertilization, soil samples were collected in two growing seasons: before the treatments, representing the initial condition of the soil (IC), and after the last application,  (2017); the total organic carbon was quantified by the wet oxidation method with external heating (Yeomans & Bremner, 1988).
The floral induction of the plants was performed 340 days after planting with 50 mL of a 1% Ethrel® solution added with calcium hydroxide (lime) at a dose of 0.35 g L -1 water (Reinhardt, Souza, and Cabral, 2001). At that time, "D" leaf samples were collected to characterize the fresh mass (FMD).
The pineapple harvest (12 fruits per plot) was performed when the fruits presented more than 70% of the peel with a yellow color. The following characteristics were evaluated: fruit mass with crown (FMWC) and without crown (FMC); fruit length (FL), and fruit diameter (FD).
The sampled fruits were subjected to the postharvest analysis of the following characteristics (AOAC, 2016): titratable soluble solids (TSS) by refractometry, using an Atago digital refractometer, model N-1α, with results expressed in °Brix; titratable acidity (TA) by titration with sodium hydroxide (0.1mol L -1 ), using 1% phenolphthalein as an indicator, with results expressed in mg of citric acid per 100 mL -1 of juice; pH, measured in anautomatic potentiometric titrator; fruit pulp Research, Society andDevelopment, v. 10, n. 11, e50101119310, 2021 (CC BY 4.0) | ISSN 2525-3409 | DOI: http://dx.doi.org/10.33448/rsd-v10i11.19310 5 The data were subjected to analysis of variance by the F test (p <0.05) using the SISVAR ® statistical software (Ferreira, 2019). The means were compared by the Scott-Knott test. We also checked for differences between treatments by applying the canonical discriminant analysis (CDA). With Wilks' Lambda test, we assessed the significance of the multivariate effects. The analyses of graphs, standardized canonical coefficients (SCC), and correlation coefficients (r), as well as the two coefficients related to the parallel discrimination rate (PDRC = SCC x r) (Baretta et al., 2005), provided information to determine which soil characteristic better discriminated between fertilizer treatments.

Changes in soil chemical properties
The chemical properties of the soil in the 0-0.20, 0.20-0.40, and 0.40-0.60 m layers were influenced (p ≤ 0.05) by the types of fertilization at the end of the pineapple cultivation period (FC) and by the time of soil usage at the end of the cultivation, compared to the initial sampling (IC). The different pineapple cultivars did not interfere with soil properties.
The soil pH at the end of the cultivation cycle, in both treatments (MF and SS), showed a significant decrease of up to 0.40 m in depth compared to the soil pH at the beginning (IC) of pineapple cultivation (Table 2). Some factors may have contributed to this, such as the use of uncured sewage sludge with acidic pH (Table 1), sludge decomposition, and the application of the nitrogen fertilizer (urea) with an acidifying effect on the soil.
The fertilization with urea increases the NH4 + content in the soil and intensifies the nitrification process, releasing 2-4 moL of H + for each mole of NH4 + in the soil solution, causing a reduction in soil pH (Tong & Xu, 2012;Latifah et al., 2018).
Sewage sludge decomposition throughout the cultivation time also favors soil acidification, as it contributes to the release of carbonic acid and non-metal oxides, such as SO4 2and NO3 -, which can form acids with water (Ociepa et al., 2017). However, several studies have reported increases in soil pH after fertilization with sewage sludge (Bittencourt et al., 2012;Latifah et al., 2018), as a result of the use of alkalinizing agents, such as CaO or Ca(OH)2, in the process of elimination of pathogens and residue stabilization. Therefore, the extent of pH changes depends on the texture and buffer capacity of the soil, as well as the type of sludge stabilization treatment. Table 2. Chemical properties of the soil at the beginning (IC) and end (FC) of the cultivation period, and changes in the chemical attributes at the end of the growing period after fertilization with sewage sludge (SS) and mineral fertilizers (MF) in the 0-0.20; 0.20-0.40, and 0.40-0.60 m depth layers. . Source: Authors.
The application of SS increased the total content of soil organic carbon (TOC) by 225, 65, and 33% at the 0-0.20; 0.20-0.40, and 0.40-0.60 m depths, respectively, at the end of the pineapple cultivation cycle (Table 2). These results corroborate those described by Nicolás et al. (2014), who observed increase rates between 100 and 120% after sludge fertilization in soils with low carbon content (<1 g kg -1 ). In the MF treatment, an increase in the TOC content was also observed for all layers, although rating only 26, 55, and 32% at the 0-0.20; 0.20-0.40, and 0.40-0.60 m depths, respectively, compared to the initial growing period. These results can be attributed to the release and decomposition of plant residues of the pineapple root system, as well as to the deposition of weeds after performing the cultural treatments.
The fertilization with SS resulted in an increase of 318 and 158% in the P content in the soil in the 0-0.20 and 0.20-0.40 m depth layers, respectively (Table 2). Rehman & Qayyum (2020) and Qayyum et al. (2015) also reported an increase in thesoil phosphorus content in response to the addition of sludge, considering the high concentration of this element in the material, the reduction in the specific adsorption of phosphates present in the soil, and the increased bioavailability. The addition of organic compounds favors the formation of functional clusters with negative surface charges in the organic matter of tropical soils (Muraishi et al., 2011). This phenomenon facilitates the formation of organomineral bonds with the solid phase of the soil (oxides) and blocks the adsorption sites, increasing the solubility of the phosphate anion (Andrade et al., 2013).
The treatments with SS and MF provided an increase of the K content in all soil layers (Table 2). This increase Furthermore, the formation of organomineral complexes between metals and humic compounds of the SS favors the displacement of Fe and Zn in the soil profile (Hashemimajd & Somarin, 2011). It is worth noting that the concentration of Zn does not constitute a restrictive factor for the agricultural use of sludge since the Zn concentration obtained was below the limit of 2,800 mg kg -1 (Brazil 2006).The increase in the content of soil Zn, after the use of sewage sludge, has been often reported in the literature (Latare et al., 2014;Nascimento et al., 2015;Li et al., 2020).
The Cu content in the soil was not influenced by the treatments at any of the evaluated depths (Table 2) Research, Society and Development, v. 10, n. 11, e50101119310, 2021 (CC BY 4.0) | ISSN 2525-3409 | DOI: http://dx.doi.org/10. 33448/rsd-v10i11.19310 8 Base saturation (V%) was not significantly influenced by the types of fertilization in the first layers (0-0.20 and 0.20-0.40 m depth). However, in the last layer, there was an increase in the base saturation of soils treated with the two types of fertilization, and this alteration was mainly attributed to the increase in the yield of the fertilizer (Table 2).
Multivariate analysis using canonical discriminants allowed to obtain the following observations for the soil chemical attributes in the 0-20 cm layer: The canonical discriminant function (CDF) 1 contributed with 87% of the discrimination between fertilization managements (Figure 2, Table 3). Sludge fertilization obtained the highest eigenvalues in comparison to mineral fertilization, and the chemical attributes that contributed the most to this discrimination were total organic carbon (TOC), total CTC, phosphorus, potassium, and iron. These attributes, presented in Table 3, had higher PDRC values and were always greater than 0.1, which is taken as the minimum for good discrimination (Azevedo Junior et al., 2019), indicating that sludge fertilization increases most of the chemical attributes of the soil over time in pineapple cultivation.  Table 3. Canonical correlation coefficient (r), standardized canonical coefficient (SCC), and parallel discrimination rate (PDRC) referring to soil chemical characteristics, within the first and second canonical discriminating function (CDF 1 and CDF 2), in sewage sludge and mineral fertilizationin initial and last moments. Bold values indicate greater component contribution to differences between treatments.

Characteristic
- For CDF 2 (with less contribution from discrimination), mineral fertilization causes a reduction in soil pH, P content, and an increase in K content in the soil (Figure 2, Table 3). These results indicated that the available forms of P supplied via mineral fertilization in tropical soils under pineapple cultivation are quickly drained into non-labile forms. However, for K, the current fertilization doses contributed to the increase of the availability of this nutrient in the soil at the end of cultivation, indicating the possibility of building fertility over the cultivation time.

Pineapple production
The production components of fruit weight with crown (FWWC), fruit weight without crown (FWC), 'D' leaf fresh matter (DFM), length (FL), and fruit diameter (FD) did not differ significantly after fertilization with different sources of fertilizers, indicating that sewage sludge fertilization provided yields equivalent to mineral fertilization. However, there were statistical differences (p≤0.05) among cultivars (Table 4). These differences were attributed to the distinct varietal characteristics of the studied pineapples.  (Table 4) (Table 4), compared to cultivars 'Vitória' and 'Pérola'. However, Spironello et al. (2010) found no fruit length differences between cultivars 'Smooth Cayenne' and 'Pérola', with an average of 15 cm. In the present study, these cultivars exhibited fruits with a diameter equal to or greater than 17 cm (Table 4).
Soil fertilization with sewage sludge produced pineapple fruits with post-harvest characteristics similar to those of mineral fertilization, except for the cultivar 'IAC Fantástico', which presented a higher content of soluble solids (ºBrix) in the fertilization with SS. However, there was a statistical difference (p ≤ 0.05) between cultivars for pulp and peel firmness, being greater in cultivars 'MD-2' and 'IAC Fantástico' (Table 4) and characterizing, according to Berilli et al. (2011), greater resistance to the industrial processing acceptance of these cultivars. Cultivars 'Smooth Cayenne', 'Vitória', and 'Pérola' showed lower pulp and peel firmness and did not differ statistically from each other.
According to Berilli et al. (2011), the optimal values of soluble solids for pineapple are between 14 and 16 ºBrix for good quality fruits destined for in natura consumption. In this context, most of the cultivars used in the study showed good quality for fresh consumption, except the cultivar 'MD-2', whose fruits had approximately 12 ºBrix. This condition was considered minimal for acceptance by consumers. Fassinou Hotegni et al. (2016) report that the quality of the pineapple fruits is essential for their acceptance by consumers; the fruits need to reach minimum requirements -pulp TSS of at least 12 ºBrix and weight of at least 0.7 kg.
The titratable acidity (TA, in % citric acid) was higher in the cultivar 'Smooth Cayenne' when compared to the others.
Cultivars 'Vitória' and 'Smooth Cayenne' presented the lowest pH values in relation to the others and, therefore, more acidic pulps (3.77 and 3.72, respectively). The pH obtained for the cultivar 'Smooth Cayenne' was higher than that found by Viana et al. (2013), which corresponded to 3.29 ± 0.02. For the cultivar'Vitória', Silva et al. (2012) found values with intervals from 3.5 to 3.8, similar results to those of the present study. Cultivars 'MD-2', 'IAC Fantástico', and 'Pérola'presented a pH range from 4.09 to 4.24 and did not differ statistically from each other ( Table 4).
The ratio between soluble solids and titratable acidity (TSS/TA) was lower in cultivars 'Smooth Cayenne' and 'MD-2' (Table 4). This fact possibly occurred due to the higher acidity associated with the lower ºBrix observed in these cultivars.
However, cultivars 'Pérola' and 'Vitória' presented the highest TSS/TA ratio. This characteristic is related to the sensation of sweetness, producing fruits with sweet pulp. These results are in agreement with those found by other authors (Silva et al., 2012;Viana et al., 2013;Berilli et al., 2014). Organic fertilization in pineapples has the potential to replace mineral fertilization (Darnaudery et al., 2018;Mahmud et al., 2018). Rothé et al. (2019) showed that organic fertilization is possible, even if applied only at planting (poultry feathers, blood meal, and composted manures), and that the average fruit weight was similar (organic fertilization= 762.6 g ± SE 19.0 and mineral fertilization = 807.4 g ± SE 17.7) to that of mineral fertilization with urea (200 kg ha -1 of N) and potassium sulfate (300 kg ha -1 K). Darnaudery et al. (2018) also showed that NPK fertilization could be replaced by organic fertilizers as well as by integrated fertilization. Pineapple growth was slower with organic fertilization (Mucuna pruriens green manure incorporated into the soil and foliar applications of sugarcane vinasse from a local distillery, rich in K -14.44 g L -1 ), with 199 days after planting vs. 149 days for integrated fertilization (M. pruriens green manure: 240.03 kg ha -1 N, 18.62 kg ha -1 P, and 136.11 kg ha -1 K, incorporated into the soil and a half-dose of NPK fertilizer) or conventional fertilization (NPK fertilizer at the recommended doses of 265.5 kg ha -1 N, 10.53 kg ha -1 P, and 445.71 kg ha -1 K), and fruit yield was lower, with 47.25 t ha -1 vs. 52.51 and 61.24 t ha -1 , probably because the organic fertilization provided an early increase in soil mineral N, whereas the N requirement is much higher at four months after planting. The yield obtained in this study was higher and/or similar to those found in the literature. Cardoso et al. (2013) obtained a yield of 65 t ha -1 in a study conducted with the cultivar 'Vitória' at the same planting density (76,923 plants ha -1 ).
However, Guarçoni and Ventura (2011)  The results obtained indicate that the use of sewage sludge as a nitrogen source is equivalent to mineral fertilization in the production and nutrition of all pineapple cultivars, providing a positive effect on soil attributes, reducing the consumption of mineral fertilizers, contributing to production.

Conclusion
Sewage sludge can be used in pineapple crops as a source of nitrogen in replacement to mineral fertilization. The fertilization with sewage sludge promoted the reduction of pH and increased the levels of organic carbon, P, Ca, Fe, and Zn in the 0-0.4 m soil layer. Regardless of the fertilizer source, the cultivar 'Smooth Cayenne' obtained the maximum yield (125 t ha -1 ), followed by pineapple cultivars 'MD-2' and 'IAC Fantástico', with intermediate yields (98 and 90 t ha -1 , respectively), and cultivars 'Pérola' and 'Vitória', with lower yields than the others (84 and 81 t ha -1 , respectively).
The organic fertilization with sewage sludge does not interfere with the physicochemical characteristics of the fruits compared to mineral fertilization.
The use of sewage sludge in agriculture can be made possible with the preparation of future studies that identify the mineralization rate of nutrients for cultivated plant species, enabling the recommendation of balanced doses of organic or organomineral fertilizers based on sludge, and the adoption of agricultural practices that contribute to environmental and economic sustainability of society and rural properties.