Ecophysiology of Soursop Seedlings Irrigated with Fish Farming Effluent under NPK Doses

Abstract

Soursop (Annona muricata L.) is a tropical fruit grown in the semi-arid region of Brazil, where problems of quantitative and qualitative scarcity of water for irrigation are frequent. Using alternative water sources, such as fish farming effluents, can increase water availability; however, it presents risks due to its high salinity levels. We aimed to evaluate the effect of irrigation with saline fish farming effluent and NPK doses on soursop seedlings’ ecophysiology. We conducted a greenhouse experiment using a randomized complete block design with a 2 × 5 factorial scheme. The factors consisted of two irrigation water sources (local supply water with 0.5 dS m⁻¹ and fish farming effluent with 3.5 dS m⁻¹) and five doses of NPK (25%, 50%, 75%, 100%, and 125% of the fertilizer recommendation of 100:300:150 mg dm⁻³ of N:P₂O₅:K₂O for soil). The soursop seedlings showed the best growth results for plant height, stem diameter, and shoot dry mass when irrigated with low-salinity water at 95% of the recommended NPK dose. However, under saline stress, the soursop seedlings showed optimal growth when fertilized with 69% of NPK dose. We recommend the following NPK fertilization for soursop seedlings: 95:285:143 mg dm⁻³ of N:P₂O₅:K₂O for those irrigated with low-salinity water and 69:207:104 mg dm⁻³ for those irrigated with fish farm effluent. Irrigating with fish farm effluent can be a practical option for soursop seedlings as it can help save fertilizers and promote environmental sustainability.

1. Introduction

The soursop tree (Annona muricata L.) is a tropical plant native to Central and South America. Soursop is a significant fruit species in the Annonaceae family, belonging to the genus Annona which comprises around 119 species [1]. It is widely distributed across many regions of the planet, but the majority of the species of this genus are found in tropical America and central Africa [2]. In Brazil, soursop fruits are consumed fresh or processed, and the demand for soursop fruits and byproducts has increased in the last 10 years due to the nutritional and medicinal value of the roots, leaves, fruits, and seeds [3,4,5]. Soursop is widely cultivated in the northeastern region of Brazil, mainly in the semi-arid region, which faces severe problems due to irrigation with saline water [6,7,8].

The shortage of water resources and the increased demand for water use drive the search for alternatives to meet crop water needs through irrigation. To ensure water savings in crop production, fish farming effluent can be used as an alternative source for irrigation [9]. The reuse of wastewater, contributing to the sustainable management of liquid waste, is pointed out as a viable alternative to increase the offering of water in agriculture, especially in climatic zones of greater water scarcity [10]. Most crops are negatively influenced by high levels of salts in the soil solution, limiting their development and yield due to morphological and physiological changes caused by saline stress [8,11,12]. The use of lower-quality water in agriculture depends on the species’ tolerance to salinity, the management of saline water in irrigation, fertilization, and other cultural practices aiming to reduce the effects of salinity on the environment [6]. However, the low availability of quality water for irrigation in semi-arid regions has forced farmers to use lower quality water for crop irrigation due to the constant population growth and the demand for food, making it necessary, therefore, to develop sustainable agricultural production systems with saline wastewater [10]. Cultivation in a protected environment is an alternative to using saline wastewater, minimizing the impacts of salinization on the environment. The production of seedlings of fruit species is a protected cultivation that guarantees the sustainability of orchard renewal [9]. However, the use of wastewater needs to be studied further, especially regarding the use of fertilizers.

According to Cavalcante et al. [6], soursop is moderately tolerant to salts during initial growth, tolerating irrigation with saline water up to 3.0 dS m⁻¹. Nobre et al. [7] verified that the accumulation of phytomass in the shoot and root of the rootstock Morada decreases with the increasing salinity of the irrigation water. However, water with up to 1.5 dS m⁻¹ of electrical conductivity can be used to produce grafted seedlings of the ‘Crioula’ soursop type. After grafting, the authors observed that the rate of seedling establishment is drastically affected by salinity, with death occurring in all grafted seedlings submitted to salinity higher than 2.5 dS m⁻¹. According to results obtained by [13], the death of seedlings is related to the sensitivity to the salinity of young and non-acclimated soursop shoots, which accumulate large concentrations of Na⁺ and Cl⁻ in their tissues.

In soursop, the studies on the interaction between salinity and fertilization involved a single nutrient, nitrogen. Veloso et al. [14] found that the interaction between nitrogen doses and water salinity levels did not affect the production phase of soursop seedlings of the Morada cultivar. In that research, N doses of 70, 100, and 130 mg dm⁻³ were evaluated, and soursop plants did not respond to increasing N doses starting at 70 mg dm⁻³ when irrigated with saline water from 0.3 to 3.5 dS m⁻¹. Silva et al. [8] evaluated soursop’s different nitrogen sources and salinity levels. However, there was no significant effect of N sources used on growth, gas exchange, and chloroplast pigment concentration, regardless of salinity used (0.3–3.5 dS m⁻¹). Further studies on fertilizer management in soursop plants exposed to salinity are needed, especially to evaluate more nutrients, such as phosphorus and potassium.

We hypothesized that plants irrigated with fish farming effluent may require less nutrients than plants irrigated with low-salinity water. We evaluated the ecophysiology of soursop seedlings submitted to irrigation with supply water and saline fish farming effluent as a function of NPK doses.

2. Materials and Methods

2.1. Location and Plant Material

We conducted an experiment in a greenhouse in Mossoró, RN, Brazil at the UFERSA (Universidade Federal Rural do Semi-Árido). The experiment was carried out from April to July 2021, lasting 90 days. During the experiment, the mean values of the maximum and minimum relative humidity and temperature were 87% and 23% and 43 °C and 20.3 °C, respectively. The design was a randomized block in a 2 × 5 factorial scheme, with four repetitions and two seedlings per repetition, totaling 80 plants. We used local supply water (SW, control) and fish farming effluent (FFE) for irrigation and five percentages of the NPK recommendation (25%, 50%, 75%, 100%, and 125%).

We produced soursop seedlings using seeds. We obtained seeds of the Morada cultivar from ripe, healthy fruit bought at a local supermarket. We chose the Morada cultivar because it is one of the most widely planted in the northeastern region of Brazil, along with the Lisa and Blanca cultivars; however, Morada is preferred because it has fewer but larger fruits per plant, which reduces labor costs during harvesting and bagging [2]. We extracted the seeds manually, washed them in running water, and laid them on paper towels in the shade to dry for a week. Subsequently, the dormancy-breaking process was performed according to the methodology of the Rules for Seed Analysis [15]. Sowing occurred in bags with a capacity of 2.0 dm³, using three seeds 1.5 cm deep. Then, 20 days after the emergence, we performed thinning, and only one plant remained per bag. The seedlings’ exposure to pests and diseases was preventively evaluated daily but was not observed during the experiment.

2.2. Soil Characteristics and Fertilization

We collected Ultisol soil [16], which corresponds to an Argissolo Vermelho-Amarelo latossólico according to the Brazilian Soil Classification System [17], from an untouched area in the Alagoinha district, Mossoró, Rio Grande do Norte State, Brazil. The soil samples were collected in the 0.0–30.0 cm layer, crushed, sieved (4 mm), and characterized for physical and chemical attributes following the methodology of [18] (Table 1).

Subsequently, soil acidity was corrected with calcium hydroxide (Ca(OH)₂), with 54% calcium, to achieve a base saturation of 90%. The soil was fertilized three times, at the foundation, at 30 days of growth, and at 60 days of growth, according to the proportions recommended by [19]. For the 100% NPK dose, 300 mg of P₂O₅, 150 mg of K₂O, and 100 mg of N were added per dm³ of soil through fertigation, using Urea (45% N), Potassium Chloride (60% K₂O), and Monoammonium Phosphate (12% N and 61% P₂O₅). Micronutrient fertilization was performed twice by foliar application, at 30 and 60 days, with the Liqui-Plex Fruit^® fertilizer, at 3 mL L⁻¹ of syrup (Table 2).

2.3. Irrigation Management

All irrigation water was collected and stored in plastic containers, each holding 150 L. Irrigation water comprised local supply water and fish farming effluent from tilapia breeding in the UFERSA-fish farming sector (Table 3).

After soil preparation, we performed irrigation to ensure that the soil remained close to maximum water retention. Subsequently, we performed irrigation once a day to keep the soil moist and close to maximum retention capacity based on the lysimetric drainage method. The irrigation depth applied was increased by a leaching fraction (LF) of 15% every 30 days. We obtained the applied volume (AV) per bag, as indicated in Equation (1), using the difference between the previously applied depth (PD) and the average drainage (D) divided by the number of containers (n).

(1)$AV=\frac{PD-D}{n\left(1-LF\right)}$

We applied 4.52 L of water per plant, corresponding to an application of 1.45 g of salts for plants irrigated with water of 0.5 dS m⁻¹ and 10.13 g of salts for those irrigated with effluent of 3.5 dS m⁻¹. We applied another leaching fraction (15%) 90 days after sowing. We collected the drained volume to determine the electrical conductivity of the drainage water (ECd) using a bench conductivity meter, with values in dS m⁻¹ adjusted to the temperature of 25 °C and pH by a bench pH meter. The electrical conductivity of the saturation extract (ECse) (Table 4) was determined using Equation (2), proposed by [20] for medium-textured soils.

(2)$ECse=\frac{ECd}{2}$

2.4. Growth and Phytomass

At 90 days after sowing, we evaluated the seedling’s height, stem diameter, primary root length, and number of leaves. We measured the seedling’s height using a graduated ruler from the ground up to the insertion of the apical meristem, with the data expressed in cm. The stem diameter of the seedlings was determined using a digital caliper at 1.0 cm from the soil surface, and the readings were expressed in mm. We determined the number of leaves by counting each plant’s fully expanded green leaves. After the growth and physiological analyses, we collected the seedlings. We sectioned them into shoot and root parts, packed them in Kraft paper bags, placed them in an oven with forced air circulation at 65 °C until they reached a constant weight, and weighed them on an analytical scale (0.0001 g) to obtain the shoot dry mass and the root dry mass, with the results expressed in g per plant.

2.5. Leaf Nutrient Concentration

The shoot dry matter was ground in a Willey-type steel mill, with subsequent storage in labeled plastic bags for analysis. In the laboratory, the material underwent wet digestion (H₂SO₄ 98% + H₂O₂ 98%) in an open system to determine the total foliar nitrogen (N) concentrations by the Kjeldahl method. Nitric acid digestion (HNO₃ 65%) in a microwave oven was performed to obtain the extract used in the reading of total foliar concentrations of phosphorus (P), potassium (K⁺), and sodium (Na⁺) according to the procedures described by [18], with readings performed in Inductively Coupled Plasma (ICP). With the data, the number of grams per plant and the Na⁺/K⁺ ratio were determined.

2.6. Leaf Gas Exchange and Chlorophyll a Fluorescence

We evaluated the seedling’s leaf gas exchange 90 days after sowing from 7:00 a.m. to 9:00 a.m. The evaluations were made on the fully expanded leaves located in the upper third of each plant with a portable infrared gas analyzer (IRGA), model LCPro + Portable Photosynthesis System^® (ADC Bio Scientific Limited, Hoddesdon, UK) with temperature control at 25 °C, irradiance of 1200 µmol photons m⁻² s⁻¹, and airflow of 200 mL min⁻¹, in order to obtain the net photosynthesis (A_N) in µmol m⁻² s⁻¹, transpiration (E) in mmol of H₂O m⁻² s⁻¹, and stomatal conductance (gs) in mol of H₂O m⁻² s⁻¹ [21]. Together with leaf gas exchange analyses, we assessed chlorophyll fluorescence using an Opti Science model OS5p pulse-modulated fluorometer using the Fv/Fm protocol for assessments under dark conditions, and the maximum quantum efficiency of PSII (Fv/Fm) was estimated [21]. In addition, evaluations were made under light conditions using a modulated pulse fluorometer using the Yield protocol. To obtain the initial fluorescence before the saturation pulse (F′), maximum fluorescence after adaptation to saturating light (Fm′), electron transport rate (ETR), and the current quantum efficiency of photosystem II (PSII) (Y) were measured. From these data, we determined the minimum fluorescence of the illuminated plant tissue (Fo′) [22], the photochemical extinction coefficient using the lake model (qL), the regulated photochemical extinction quantum yield (Y_NPQ), and the unregulated photochemical extinction quantum yield (Y_NO) [23].

2.7. Statistical Analysis

The data were submitted to analysis of variance using the F test; the interaction between the factors and the isolated factors were analyzed; in cases of significance, a Student’s t-test was applied for the irrigation water factor and regression for the NPK doses factor, at a significance level of 5%, with the aid of SISVAR^® 5.3 statistical software [24].

3. Results

3.1. Growth and Phytomass

There was a significant interaction between irrigation water and NPK doses for the plant height (p < 0.001), stem diameter (p < 0.05), number of leaves (p < 0.001), root length (p < 0.001), and shoot dry mass (p < 0.01) of soursop seedlings (Table 5). For the root dry mass of soursop seedlings, the isolated factors, irrigation water (p < 0.001) and NPK doses (p < 0.001), had a significant effect (Table 5).

The plant height of soursop was greater in seedlings irrigated with supply water than in those irrigated with fish farming effluent at all doses of NPK (Figure 1A and Figure 2). The greatest PH of soursop irrigated with supply water was 29.60 cm at a dose of 85.56% NPK (Figure 1A). The greatest PH of soursop irrigated with fish farming effluent was 23.46 cm at a dose of 68.46% NPK (Figure 1A). Observing the best results for soursop plant height, it can be seen that irrigation with fish farming effluent reduced plant height by 20.74% in comparison to supply water (Figure 1A).

The stem diameter (SD) of soursop was greater in seedlings irrigated with supply water than in those irrigated with fish farming effluent only at doses of 50% and 125% of NPK (Figure 1B and Figure 2). The highest SD of soursop irrigated with supply water was 4.40 mm at 103.50% NPK (Figure 1B). The highest SD of soursop irrigated with fish farming effluent was 3.76 mm at a dose of 59.33% NPK (Figure 1B). Observing the best SD results of soursop, it can be seen that the plants irrigated with fish farming effluent possessed reduced diameters (by 14.55%) in comparison to those irrigated with supply water (Figure 1B).

The number of leaves (NL) of soursop was greater in seedlings irrigated with supply water than in those irrigated with fish farming effluent at all NPK doses (Figure 1C and Figure 2). For the number of leaves of soursop irrigated with supply water, there was no adjustment of the regression models tested, with an average of 12.6 leaves per plant for all doses of NPK. The highest and lowest NL of soursop irrigated with supply water were 13.25 and 11.50 leaves on average at doses of 50% and 25% NPK, respectively (Figure 1C). The highest NL of soursop irrigated with fish farming effluent was 11.07 leaves on average at 63.04% NPK (Figure 1C). Observing the best results for soursop, irrigation with fish farming effluent reduced the number of leaves by 16.45% compared to supply water (Figure 1C).

The root length (RL) of soursop was greater in seedlings irrigated with supply water than in those irrigated with fish farming effluent only at a dose of 125% NPK (Figure 1D). Regarding the root length of soursop irrigated with supply water, there was no adjustment of the regression models tested, with an average of 21.21 cm for all doses of NPK. The highest and lowest RL of soursop irrigated with supply water were 22.58 and 20.00 cm for the 100 and 50% NPK doses, respectively (Figure 1D). The highest RL of soursop irrigated with fish farming effluent was 21.35 cm at 46.29% NPK (Figure 1D). Observing the best RL results for soursop, the plants irrigated with fish farming effluent displayed reduced root lengths (by 5.45%) when compared to those irrigated with supply water (Figure 1D).

The shoot dry mass (SDM) of soursop was greater in seedlings irrigated with supply water than in those irrigated with fish farming effluent at all doses of NPK (Figure 1E). The highest SDM of soursop irrigated with supply water was 2.13 g per plant at 95.50% NPK (Figure 1E). The highest SDM of soursop irrigated with fish farming effluent was 1.19 g per plant at a dose of 79.50% NPK (Figure 1E). Observing the best results of SDM for soursop, the plants irrigated with fish farming effluent had reduced mass (by 44.13%) when compared to those irrigated with supply water (Figure 1E).

The root dry mass (RDM) of soursop irrigated with fish farming effluent decreased by 52.73% in relation to seedlings irrigated with supply water, regardless of NPK dose (Table 5). The best NPK dose for the root dry mass of soursop seedlings was 71.25%, obtaining an average of 0.69 g per plant, regardless of the irrigation water used (Figure 1F).

3.2. Leaf Nutrient Concentration

There was a significant interaction between irrigation water and NPK doses for nitrogen accumulation (p < 0.05), phosphorus accumulation (p < 0.05), potassium accumulation (p < 0.001), and the sodium–potassium ratio (p < 0.001) of soursop seedlings (Table 6). For sodium accumulation in soursop seedlings, there was a significant effect of the isolated factors of irrigation water (p < 0.001) and NPK doses (p < 0.001) (Table 6).

The nitrogen (N) accumulation in soursop trees was higher in seedlings irrigated with local supply water than in those irrigated with fish farming effluent across all NPK doses, except for the 25% NPK dose, where the values were similar (Figure 3A). The highest N accumulation in soursop trees irrigated with supply water was 57.55 mg per plant, at the 87.72% NPK dose (Figure 3A). The highest N accumulation in soursop trees irrigated with fish farming effluent was 31.36 mg per plant, at the 71.39% NPK dose (Figure 3A). Examining the best N accumulation results in soursop trees, plants irrigated with fish farming effluent showed a 46.13% reduction in nitrogen accumulation compared to those irrigated with local supply water (Figure 3A).

Phosphorus (P) accumulation in soursop trees was higher in seedlings irrigated with local supply water than in those irrigated with fish farming effluent across all NPK doses (Figure 3B). The highest P accumulation in soursop trees irrigated with local supply water was 8.13 mg per plant, at the 104.90% NPK dose (Figure 3B). The highest P accumulation in soursop trees irrigated with fish farming effluent was 3.26 mg per plant, at the 66.92% NPK dose (Figure 3B). Examining the best P accumulation results in soursop trees, plants irrigated with fish farming effluent showed a 59.60% reduction compared to those irrigated with local supply water (Figure 3B).

Potassium (K⁺) accumulation in soursop trees was higher in seedlings irrigated with local supply water than in those irrigated with fish farming effluent across all NPK doses (Figure 3C). The highest K⁺ accumulation in soursop trees irrigated with local supply water was 42.47 mg per plant, at the 96.85% NPK dose (Figure 3C). The highest K⁺ accumulation in soursop trees irrigated with fish farming effluent was 20.84 mg per plant, at the 71.59% NPK dose (Figure 3C). Analyzing the best K⁺ accumulation results in soursop trees, plants irrigated with fish farming effluent showed a 50.68% reduction compared to those irrigated with local supply water (Figure 3C).

The sodium (Na⁺) accumulation in soursop trees irrigated with fish farming effluent decreased by an average of 30.04% compared to seedlings irrigated with local supply water, regardless of the NPK dose (Table 6). The NPK dose at which soursop seedlings accumulated the most Na⁺ was 64.60%, resulting in an average of 10.00 mg per plant, regardless of the irrigation water used (Figure 3D).

The Na⁺/K⁺ ratio in soursop trees was higher in seedlings irrigated with fish farming effluent than in those irrigated with local supply water across all NPK doses, except for the 25% NPK dose, where they were similar (Figure 3E). For the Na⁺/K⁺ ratio in soursop trees irrigated with local supply water, a decreasing linear trend was observed. The highest and lowest Na⁺/K⁺ ratios in soursop trees irrigated with local supply water were 0.42 and 0.18 at the 25% and 125% NPK doses, respectively, representing a decrease of 57.14% in the Na⁺/K⁺ ratio (Figure 3E).

Regarding the Na⁺/K⁺ ratio in soursop trees irrigated with fish farming effluent, the tested regression models did not adjust, with an average of 0.44 across all NPK doses. The highest and lowest Na⁺/K⁺ ratios in soursop trees irrigated with fish farming effluent were 0.60 and 0.30 at the 50% and 100% NPK doses, respectively (Figure 3E). According to the best Na⁺/K⁺ ratio results of soursop, the plants irrigated with fish farming effluent had increased Na⁺/K⁺ ratios of at least 40%, in comparison to the plants that used supply water (Figure 3E).

3.3. Leaf Gas Exchange and Chlorophyll a Fluorescence

The interaction between irrigation water and NPK doses was significant for the CO₂ assimilation rate (p < 0.05), stomatal conductance (p < 0.01), and transpiration (p < 0.01) of soursop seedlings (Table 7). For the maximum quantum efficiency of PSII in soursop seedlings, there was a significant effect only for irrigation water (p < 0.001) (Table 7).

The maximum quantum efficiency of PSII (Fv/Fm) of soursop irrigated with fish farming effluent decreased by an average of 5.40% compared to seedlings irrigated with supply water, regardless of the dose of NPK (Table 7).

The CO₂ assimilation rate (A_N) of soursop was higher in seedlings irrigated with supply water than in those irrigated with fish farming effluent only at doses of 25, 100, and 125% of NPK (Figure 4A). For the A_N of soursop irrigated with supply water, there was no adjustment of the regression models tested, with a mean of 5.56 μmol (CO₂) m⁻² s⁻¹ for all doses of NPK. The highest and lowest A_N of soursop irrigated with supply water were 7.05 and 4.87 μmol (CO₂) m⁻² s⁻¹ at doses 25 and 50% of NPK, respectively (Figure 4A). For the A_N of soursop irrigated with fish farming effluent, there was a linear decreasing trend. The highest and lowest A_N of soursop irrigated with fish farming effluent were 4.56 and 1.97 μmol (CO₂) m⁻² s⁻¹ in doses of 25 and 125% of NPK, respectively, representing a decrease of 56.80% in A_N (Figure 4A). Looking at the best A_N results of soursop, plants irrigated with fish farming effluent decreased A_N by at least 35.32% when compared to those irrigated with supply water (Figure 4A).

The stomatal conductance (gs) of soursop was higher in seedlings irrigated with supply water than in those irrigated with fish farming effluent at all NPK doses, except for the dose of 50% NPK, in which they were similar (Figure 4B). For the gs of soursop irrigated with supply water, there was no adjustment of the regression models tested, with a mean of 0.06 mol (H₂O) m⁻² s⁻¹ for all doses of NPK. The highest and lowest gs of soursop irrigated with supply water were 0.08 and 0.05 mol (H₂O) m⁻² s⁻¹ at doses of 25% and 50% of NPK, respectively (Figure 4B). For the gs of soursop irrigated with fish farming effluent, there was a linear decreasing trend. The highest and lowest gs of soursop irrigated with fish farming effluent were 0.042 and 0.012 mol (H₂O) m⁻² s⁻¹ at 25% and 125% NPK, respectively, representing a decrease of 71.77% in gs (Figure 4B). The plants irrigated with fish farming effluent had decreased gs (by at least 47.50%) when compared to those irrigated with supply water (Figure 4B).

The transpiration (E) of soursop was higher in seedlings irrigated with supply water than in those irrigated with fish farming effluent at all doses of NPK (Figure 4C). There was no regression model adjustment for the E of soursop irrigated with supply water, with a mean of 1.84 mmol (H₂O) m⁻² s⁻¹ for all doses of NPK. The highest and lowest E of soursop irrigated with supply water were 2.35 and 1.55 mmol (H₂O) m⁻² s⁻¹ at doses of 25 and 50% of NPK, respectively (Figure 4C). There was a linear decreasing trend for the E of soursop irrigated with fish farming effluent. The highest and lowest E of soursop irrigated with fish farming effluent were 1.50 and 0.57 mmol (H₂O) m⁻² s⁻¹ in doses of 25 and 125% of NPK, respectively, configuring a decrease of 62.00% in E (Figure 4C). Observing the best results of the E of soursop, irrigation with fish farming effluent decreased the E by at least 36.17% when compared to irrigation with supply water (Figure 4C).

The interaction between irrigation water and NPK doses was significant for the electron transport rate (p < 0.05), photochemical extinction coefficient (p < 0.01), and unregulated photochemical extinction quantum yield (p < 0.05) of soursop seedlings (Table 8). Regarding the PSII quantum efficiency and regulated photochemical extinction quantum yield (Y_NPQ) of soursop seedlings, there was a significant effect only for NPK doses (p < 0.05) (Table 8).

The highest PSII quantum efficiency (Y) of soursop was obtained at the NPK dose of 72.5%, with Y equal to 0.63, regardless of the irrigation water used (Figure 5A).

The electron transport rate (ETR) of soursop was higher in seedlings irrigated with supply water than in those irrigated with fish farming effluent only at a dose of 75% NPK (Figure 5B). For the ETR, there was no significant adjustment of the regression models tested, with values ranging from 40.8 to 55.1 µmol (photons) m⁻² s⁻¹ and an average among the NPK doses of 36.6 µmol (photons) m⁻² s⁻¹ (Figure 5B). The ETR of soursop irrigated with fish farming effluent showed a quadratic adjustment, with the lowest ETR of 24.5 µmol (photons) m⁻² s⁻¹ at the dose of 83.2% NPK (Figure 5B). The ETR of soursop in plants irrigated with fish farming effluent under the dose of 83.2% of NPK decreased by 33.1% in relation to the average ETR obtained in plants irrigated with supply water (Figure 5B).

The photochemical extinction coefficient (qL) of soursop was higher in seedlings irrigated with supply water than in those irrigated with fish farming effluent only at a dose of 75% NPK (Figure 5C). At a dose of 125%, the photochemical extinction coefficient of soursop was higher in seedlings irrigated with fish farming effluent than in seedlings irrigated with supply water (Figure 5C). For the qL of soursop irrigated with supply water, there was a linear increasing trend. The lowest and highest qL of soursop irrigated with supply water were 0.0061 and 0.0111 at doses of 25 and 125% of NPK, respectively, showing an increase of 81.98% in qL (Figure 5C). In the qL of soursop irrigated with fish farming effluent, there was a quadratic adjustment, verifying the highest qL at the NPK dose of 50%, with a qL of 0.0101 (Figure 5C). Considering the best results for soursop qL, irrigation with fish farming effluent decreased plant qL by 9.01% when compared to supply water (Figure 5C).

The lowest regulated photochemical extinction quantum yield (Y_NPQ) of soursop was obtained at the NPK dose of 70%, with Y_NPQ equal to 0.415, regardless of the irrigation water used (Figure 5D). At the dose of 125%, the unregulated photochemical extinction quantum yield (Y_NO) of soursop was higher in seedlings irrigated with fish farming effluent than in those irrigated with supply water (Figure 5E). For the Y_NO of soursop irrigated with supply water, there was a linear decreasing trend. The highest and lowest Y_NO of soursop irrigated with supply water were 0.090 and 0.060 at 25% and 125% NPK, respectively, representing a reduction of 33.33% in Y_NO (Figure 5E). In the Y_NO of soursop irrigated with fish farming effluent, there was a quadratic adjustment, verifying the lowest Y_NO at the dose of 50% of NPK, with a Y_NO of 0.092 (Figure 5E). Analyzing the results of the Y_NO of soursop obtained at the dose of 50% NPK, irrigation with fish farming effluent increased the Y_NO by 11.92% compared to supply water (Figure 5E).

4. Discussion

The irrigation of crops with saline effluents can result in numerous damages to plants and the soil; however, if well-managed and controlled, it becomes a viable alternative that contributes both to saving better quality water and fertilizers and to the reuse of effluents, which are rich in essential nutrients for plants. Research to assess the positive and negative impacts of effluent reuse in agriculture is fundamental, especially in areas with water scarcity. We assessed the ecophysiology of soursop seedlings subjected to irrigation with saline fish farming effluent at different NPK doses. We found that, when growing soursop plants irrigated with low-salinity water (0.5 dS m⁻¹), NPK fertilization increased the initial soil salinity from 0.11 dS m⁻¹ to values of 1.2, 2.5, 3.3, 4.2, and 4.8 dS m⁻¹ at doses of 25%, 50%, 75%, 100%, and 125% of the NPK recommendation, respectively. The saline effect of the fertilizers was toxic to soursop plants due to the reduction in osmotic potential, as can be seen by the quadratic adjustment of the regression model for the growth variables. The best results for plant height, stem diameter, and shoot dry mass for the soursop seedlings under these conditions (0.5 dS m⁻¹) were observed at the average dose of 95% of the NPK recommendation, which corresponds to 95:285:143 mg dm⁻³ of N:P₂O₅:K₂O. The dose obtained for the highest seedling growth is close to that obtained for the highest nitrogen, phosphorus, and potassium accumulations, which occurred at the average dose of 96.5% of the NPK recommendation. This difference of 1.5% of N:P₂O₅:K₂O between the optimal dose for growth and nutrient accumulation can be attributed to luxury consumption, as it did not bring any gains to seedling growth.

The osmotic effect results from the high concentration of salts in the root zone, decreasing osmotic and soil water potential and thereby restricting water availability to the plant [25]. According to Oliveira et al. [26], the plant’s inability to perform osmotic adjustments results in water deficiency induced by the osmotic effect, which causes morphological and anatomical alterations in plants, as observed in the soursop seedlings.

Our results revealed that in the cultivation of soursop plants irrigated with fish farming effluent (3.5 dS m⁻¹), the salinity of the effluent combined with NPK fertilization increased the initial soil salinity from 0.11 dS m⁻¹ to values of 5.1, 3.8, 4.6, 5.6, and 6.1 dS m⁻¹ at doses of 25%, 50%, 75%, 100%, and 125% of the NPK recommendation, respectively. Under saline stress, we found the best results for plant height, stem diameter, and shoot dry mass occurred in soursop seedlings fertilized with 69% of the NPK recommendation, which corresponds to 69:207:104 mg dm⁻³ of N:P₂O₅:K₂O. The dose obtained for the highest seedling growth is close to that obtained for the highest nitrogen, phosphorus, and potassium accumulations, which occurred at an average of 70.0% of the NPK recommendation. As observed in plants under saline stress, this difference of 1.0% of N:P₂O₅:K₂O between the optimal dose for growth and nutrient accumulation can also be attributed to luxury consumption, as it did not bring any gains to seedling growth.

These results confirm our hypothesis that soursop seedlings subjected to irrigation by saline fish farming effluent need less nutrients than those irrigated with low-salinity water to achieve their optimum growth and photosynthetic performance in each specific salinity condition. This response of requiring less nutrients is partly due to the reduction in seedling growth under conditions of salt stress. When comparing the best results for plant height, stem diameter, and shoot dry mass in seedlings irrigated with low-salinity water and fish farming effluent, there was a decrease in the growth of seedlings irrigated with fish farming effluent by approximately 20.74%, 14.55%, and 44.13%, respectively. We observed that the shoot growth of the seedlings decreased by an average of 25.5%, which coincides with a reduction in nutrient absorption of approximately 26.5%, compared to those cultivated with fish farming effluent in low-salinity water.

Our findings showed that the lowest soil salinities in the irrigated soil with fish farming effluent occurred at doses of 50% and 75% of the NPK recommendation, matching with the highest nutrient absorption and extraction by the seedlings. A crucial point to note is that these lower salinities also coincide with the highest sodium extraction from the soil. However, at the 75% NPK dose, the lowest sodium–potassium ratio (0.30) is observed. The improved growth of soursop seedlings irrigated with fish farming effluent occurs due to their ability to absorb nutrients and sodium and control the sodium–potassium ratio, i.e., to maintain ionic homeostasis. The ionic effect refers to accumulating certain specific ions, primarily Na⁺ [27,28]. Furthermore, the ionic effect causes an imbalance in plant nutrient uptake, transport, assimilation, and distribution processes [21,29,30].

In a study carried out by Veloso et al. [14], the growth of Morada soursop seedlings was evaluated under the interaction between water salinity levels (0.3 to 3.5 dS m⁻¹) and nitrogen (N) fertilization (70% to 160% of the recommended dose). According to their findings, the production of seedlings was not impacted by the factors. During the initial stage (45 days), the growth was less affected. Additionally, despite causing some reduction in growth (less than 10%), soursop seedlings can be produced with water of 2.0 dS m⁻¹. However, doses of N above 70 md dm⁻³ do not prevent the adverse effects of salinity or contribute to significant growth in the seedlings with fertilization of N. In a series of recent studies conducted by Sá et al. [21], adjustments to the recommended levels of nitrogen, phosphorus, and potassium can significantly affect the growth and productivity of certain plant species. Specifically, using saline water for irrigation can be challenging for plants such as the custard apple (Annona Squamosa L.). However, with the right nutrient balance, these plants can improve their water relations, leaf gas exchange, and ion homeostasis, leading to healthier growth and better production yields. These findings highlight the importance of understanding the specific nutrient requirements of different plant species and tailoring fertilization strategies accordingly.

Soursop plants, irrigated with fish farming effluent and fertilized with NPK doses exceeding 69% of the recommended fertilization requirements, experienced drastic reductions in growth, which coincided with a linear decrease in the rate of CO₂ assimilation (A_N), stomatal conductance (gs), and transpiration (E) of the seedlings with increasing NPK fertilization. An important fact is that the A_N of soursop plants irrigated with fish farming effluent at 50% and 75% of the NPK recommendation was similar to that of those irrigated with supply water at the same doses. However, this similarity was observed only at the 50% NPK dose for the gs and E, which coincided with the highest sodium–potassium ratio of 0.60. This finding indicates that by opening their stomata (0.038 mol (H₂O) m⁻² s⁻¹) and boosting the transpiratory flow, the soursop absorbed more sodium and accumulated it in excess. The sodium–potassium ratio of 0.60 represents a critical level for plants. To maintain a low sodium–potassium ratio, the soursop plants expended excess energy, limiting the use of photo-assimilates for growth.

The similarities in the A_N results of soursop plants irrigated with fish farming effluent and supply water at 50% and 75% of the NPK recommendation corroborated with the higher quantum efficiency of PSII (Y) of soursop at 0.63, which occurred at the 72.5% NPK dose. Under these circumstances, soursop plants subjected to salt stress exhibited lower electron transport rates, but the light energy was more effectively utilized, resulting in the higher quantum efficiency of PSII. At the 75% NPK dose, there was a decrease in the coefficient of photochemical quenching (qL), regulated quantum yield of photochemical quenching (Y_NPQ), and non-regulated quantum yield of photochemical quenching (Y_NO) compared to other NPK doses, especially doses exceeding it.

The findings of our research revealed that properly fertilized soursop plants irrigated with fish farming effluent decrease the loss of energy in the form of regulated fluorescence, meaning they decrease fluorescence quenching in PSII (Y_NPQ) and minimize the loss of energy through kinetic and resonance processes in PSII (Y_NO) [10,31]. Furthermore, the decrease in the coefficient of photochemical quenching (qL) indicates that fewer reaction centers of quinone were open [10,31], implying a greater utilization of light energy, which aligns with the results of PSII quantum efficiency (Y).

Silva et al. [8] and Capitulino et al. [32] used 100% of the recommended NPK dosage at various salinity levels in studies on the photosynthetic responses of soursop plants exposed to salinity. They found that the growth, gas exchange, concentration of photosynthetic pigments, and photochemical efficiency of soursop decreased after 110 days of irrigation with saline water starting from 1.5 dS m⁻¹. When comparing seedlings irrigated at levels of 0.5 and 3.5 dS m⁻¹, these researchers observed a decrease in stomatal conductance from 0.046 to 0.028 mol (H₂O) m⁻² s⁻¹, a decrease in transpiration from 0.70 to 0.45 mmol (H₂O) m⁻² s⁻¹, a decrease in photosynthesis from 4.02 to 1.10 µmol (CO₂) m⁻² s⁻¹, and a decrease in the maximum efficiency of photosystem II (Fv/Fm) from 0.70 to 0.67. In our study, soursop plants irrigated with fish farming effluent, which had an electrical conductivity of 3.5 dS m⁻¹, and fertilized with 75% of the recommended dosage, showed a mean value of stomatal conductance of 0.053 mol (H₂O) m⁻² s⁻¹ and a mean value of transpiration of 1.67 mmol (H₂O) m⁻² s⁻¹. The photosynthetic rate had a mean value of 3.90 µmol (CO₂) m⁻² s⁻¹ and the maximum efficiency of photosystem II had an average value of 0.68. Under low-salinity irrigation conditions, our results were superior to those obtained by those researchers. Therefore, our research demonstrated that proper fertilization of plants irrigated with saline fish farming effluent improves the photosynthetic performance of soursop seedlings.

5. Conclusions

Soursop seedlings exhibit different responses to NPK fertilization under irrigation with low-salinity water and fish farming effluent. The ideal NPK fertilization concentration for soursop seedlings irrigated with low-salinity water is 95:285:143 mg dm⁻³ of N:P₂O₅:K₂O. However, the ideal amount for those irrigated with fish farming effluent is 69:207:104 mg dm⁻³ of N:P₂O₅:K₂O. This means that plants irrigated with saline fish farming effluent require less nutrients than those irrigated with low-salinity water. Using fish farming effluent and fertilization at 69% of the recommended NPK dose positively impacts soursop seedlings’ vegetative growth and photosynthetic performance. This can be due to the efficient regulation of ion homeostasis between sodium and potassium ions, which maintains an optimal balance for the plant’s biological processes. As a result, the plants exhibit enhanced growth and better photosynthetic activity, leading to a healthier and more productive crop and more sustainable agriculture, both by saving on fertilizers and by using fish farming effluent.

Author Contributions

Conceptualization, methodology, statistical analysis, investigation, data curation, F.V.d.S.S., M.F.N., S.B.T., A.A.T.S. and N.d.S.D.; writing—original draft preparation, F.V.d.S.S., M.F.N., S.B.T., A.A.T.S., K.T.O.P., T.D.C.P., E.P.d.P., R.C.L.M. and N.d.S.D.; conceptualization, resources and writing-review and editing, T.D.C.P., K.T.O.P., R.C.L.M. and N.d.S.D.; methodology and resources, F.V.d.S.S., M.F.N., S.B.T. and P.D.F.; conceptualization and laboratory resources, F.V.d.S.S., F.d.C.d.O., A.S.d.S. and A.A.T.S.; redaction and writing-review and editing, T.D.C.P., L.d.A.S., K.T.O.P., R.C.L.M., H.A.d.A., A.S.d.M. and F.V.d.S.S. All authors have read and agreed to the published version of the manuscript.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Data is contained within the article.

Conflicts of Interest

The authors declare no conflicts of interest.

Footnotes

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Figures and Tables

Figure 1. Plant height, PH ((A) n = 4), stem diameter, SD ((B) SE, n = 4), number of leaves, NL ((C) SE, n = 4), root length, RL ((D) SE, n = 4), Shoot Dry Mass, SDM ((E) SE, n = 4), and Root Dry Mass, RDM ((F) SE, n = 8) of soursop seedlings irrigated with supply water (⸺♦⸺) and with fish farming effluent (---●---) under NPK doses, at 90 days after sowing. * = significant (p < 0.05). ns = not significant. Means of the same dose of NPK with equal letters do not differ by the Student’s t-test at 0.05 probability. Vertical bars on the means represent the standard error (SE).

Figure 2. Soursop seedlings irrigated with supply water and with fish farming effluent under NPK doses at 90 days after sowing.

Figure 3. Accumulation of nitrogen, N (A), phosphorus, P (B), potassium, K+ (C), sodium, Na+ (D), and the sodium–potassium ratio, Na+/K+ (E), in the shoot of soursop seedlings irrigated with supply water (⸺♦⸺) and with fish farming effluent (---●---) under NPK doses, at 90 days after sowing. * = significant (p < 0.05). ns = not significant. Means of the same NPK dose with equal letters do not differ by Student’s t-test at 0.05 probability. Vertical bars on the means represent the standard error (SE).

Figure 3. Accumulation of nitrogen, N (A), phosphorus, P (B), potassium, K+ (C), sodium, Na+ (D), and the sodium–potassium ratio, Na+/K+ (E), in the shoot of soursop seedlings irrigated with supply water (⸺♦⸺) and with fish farming effluent (---●---) under NPK doses, at 90 days after sowing. * = significant (p < 0.05). ns = not significant. Means of the same NPK dose with equal letters do not differ by Student’s t-test at 0.05 probability. Vertical bars on the means represent the standard error (SE).

Figure 4. CO2 assimilation rate, AN ((A) SE, n = 4), Stomatal conductance, gs ((B) SE, n = 4), and transpiration, E ((C) SE, n = 4) of soursop seedlings irrigated with supply water (⸺♦⸺) and with fish farming effluent (---●---) under NPK doses at 90 days after sowing. * = significant (p < 0.05). ns = not significant. Means of the same NPK dose with equal letters do not differ by Student’s t-test at 0.05 probability. Vertical bars on the means represent the standard error (SE).

Figure 5. PSII quantum efficiency, Y (A), electron transport rate, ETR (B), photochemical extinction coefficient, qL (C), regulated photochemical extinction quantum yield, YNPQ (D), and unregulated photochemical extinction quantum yield YNO (E) of soursop seedlings irrigated with supply water (⸺♦⸺) and with fish farming effluent (---●---) under NPK doses at 90 days after sowing. * = significant (p < 0.05). ns = not significant. Means of the same NPK dose with equal letters do not differ by Student’s t-test at 0.05 probability. Vertical bars on the means represent the standard error (SE).

Table 1

Physical and chemical characteristics of the soil.

pH	OM	P	K+	Na+	Ca2+	Mg2+	Al3+	H + Al	CEC	BS	ESP
	(%)	----- (mg dm−3) -----			-------------------- (cmolc dm−3) --------------------					--- % ---
5.3	1.7	2.1	54.2	21.6	2.7	0.9	0.0	1.8	5.6	68	2.0
ECsedS m−1		SDkg dm−3	Sand				Silt		Clay
			---------------------------- (g kg−1) --------------------------------------------
0.1		1.6	820				30		150

pH—Potential hydrogen; OM—Organic matter; ECse—Electrical conductivity of the saturation extract of the soil; SD—Soil density; CEC—Cation exchange capacity; BS—Base saturation; ESP—Exchangeable sodium percentage.

Table 2

Foliar fertilizer Liqui-Plex Fruit^®.

N	Ca	S	B	Cu	Mn	Mo	Zn−	OC
------------------------------------------------- g L−1 --------------------------------------------------								%
73.50	14.70	78.63	14.17	0.74	73.50	1.47	73.50	2.45

N—Nitrogen; Ca—Calcium; S—Sulfur; B—Boron; Cu—Copper; Mn—Manganese; Mo—Molybdenum; Zn—Zinc; OC—Organic Carbon.

Table 3

Analysis of the water used in the irrigation of soursop seedlings.

Parameters	Supply Water	Fish Farming Effluent
Potential hydrogen (pH)	7.8	8.2
Electrical conductivity (dS m−1)	0.5	3.5
Nitrogen (mg L−1)	0.1	0.3
Phosphorus (mg L−1)	0.1	0.8
Potassium (mmolc L−1)	0.3	0.7
Sodium (mmolc L−1)	6.6	16.3
Calcium (mmolc L−1)	0.3	8.9
Magnesium (mmolc L−1)	1.1	12.2
Chloride (mmolc L−1)	2.6	22.6
Carbonate (mmolc L−1)	0.2	1.2
Bicarbonate (mmolc L−1)	2.8	3.4
Sodium adsorption ratio (mmolc L−1)0.5	7.9	5.2
Chemical oxygen demand (mg L−1)	-	10.0
Biochemical oxygen demand (mg L−1)	-	135
Suspended solids (mg L−1)	-	5.6
Total solids (mg L−1)	-	31.3
Turbidity (NTU)	2.85	30.9

Table 4

Electrical conductivity of the saturation extract (ECse) and pH of the saturation extract (pHse) of the soil under irrigation with fish farming effluent and different doses of NPK.

Fertilizer Recommendation of NPK (%)	ECse (dS m−1)		pHse
	SW	FFE	SW	FFE
25	1.2	5.1	7.2	6.7
50	2.5	3.8	6.8	7.1
75	3.3	4.6	5.8	6.7
100	4.2	5.6	6.0	6.3
125	4.8	6.1	5.2	6.3

SW—Supply Water; FFE—Fish Farming Effluent.

Table 5

Summary of the F test and Student’s t-test for plant height (PH, in cm), stem diameter (SD, in mm), number of leaves (NL), root length (RL, in cm), shoot dry mass (SDM, in g), and root dry mass (RDM, in g) of soursop seedlings under irrigation with fish farming effluent and doses of NPK, 90 days after sowing.

F Test (Pr > Fc)
Variation Sources	PH	SD	NL	RL	SDM	RDM
Block	0.3604	0.2058	0.1644	0.7476	0.4827	0.4473
Water	0.0000	0.0000	0.0000	0.0000	0.0000	0.0000
NPK Doses	0.0000	0.0130	0.0003	0.0000	0.0000	0.0002
Water × NPK Doses	0.0002	0.0188	0.0005	0.0001	0.0017	0.2370
Student’s t-test (p < 0.05)
Treatments	PH	SD	NL	RL	SDM	RDM
Supply Water	27.75 a	4.13 a	12.60 a	21.21 a	1.67 a	0.55 a
Fish Farming Effluent	19.75 b	3.56 b	9.35 b	17.51 b	0.76 b	0.26 b

Means followed by equal letters in the column do not differ by Student’s t-test at 0.05 probability.

Table 6

Summary of the F test and Student’s t-test for the accumulation of nitrogen (N, mg per plant), phosphorus (P, mg per plant), potassium (K⁺, mg per plant), sodium (Na⁺, mg per plant), and the sodium–potassium ratio (Na⁺/K⁺) in the shoots of soursop seedlings under irrigation with fish farming effluent and NPK doses, 90 days after sowing.

F Test (Pr > Fc)
Variation Sources	N	P	K+	Na+	Na+/K+
Block	0.3976	0.7942	0.5030	0.1588	0.9998
Water	0.0000	0.0000	0.0000	0.0000	0.0000
NPK Doses	0.0001	0.0062	0.0000	0.0000	0.0000
Water × NPK Doses	0.0102	0.0175	0.0001	0.1405	0.0000
Student’s t-test (p < 0.05)
Treatments	N	P	K+	Na+	Na+/K+
Supply Water	45.65 a	6.74 a	34.61 a	9.52 a	0.29 b
Fish Farming Effluent	22.60 b	2.66 b	15.36 b	6.66 b	0.44 a

Means followed by equal letters in the column do not differ by Student’s t-test at 0.05 probability.

Table 7

Summary of the F test and Student’s t-test for CO₂ assimilation rate (A_N, in μmol (CO₂) m⁻² s⁻¹), stomatal conductance (gs, in mol (H₂O) m⁻² s⁻¹), transpiration (E, in mmol (H₂O) m⁻² s⁻¹), and maximum quantum efficiency of PSII (Fv/Fm) of soursop seedlings under irrigation with fish farming effluent and NPK doses, at 90 days after sowing.

F Test (Pr > Fc)
Variation Sources	AN	gs	E	Fv/FM
Block	0.2686	0.0336	0.0896	0.3842
Water	0.0000	0.0000	0.0000	0.0000
NPK Doses	0.0064	0.0002	0.0008	0.2235
Water × NPK Doses	0.0247	0.0077	0.0019	0.7459
Student’s t-test (p < 0.05)
Treatments	AN	gs	E	Fv/FM
Supply Water	5.56 a	0.060 a	1.84 a	0.722 a
Fish Farming Effluent	3.26 b	0.028 b	1.04 b	0.683 b

Means followed by equal letters in the column do not differ by Student’s t-test at 0.05 probability.

Table 8

Summary of the F test and Student’s t-test for PSII quantum efficiency (Y), electron transport rate (ETR, µmol (photons) m⁻² s⁻¹), minimum fluorescence of illuminated plant tissue (Fo′, µmol (photons) m⁻² s⁻¹), photochemical extinction coefficient (qL), regulated photochemical extinction quantum yield (Y_NPQ), and unregulated photochemical extinction quantum yield (Y_NO) of soursop seedlings under irrigation with fish farming effluent and NPK doses, at 90 days after sowing.

F Test (Pr > Fc)
Variation Sources	Y	ETR	Fo’	qL	YNPQ	YNO
Block	0.1561	0.0719	0.2490	0.3189	0.1344	0.9227
Water	0.4889	0.0211	0.1298	0.6304	0.6688	0.0537
NPK Doses	0.0187	0.3526	0.0833	0.5270	0.0178	0.3396
Water × NPK Doses	0.1574	0.0353	0.0551	0.0044	0.1789	0.0139
Student’s t-test (p < 0.05)
Treatments	Y	ETR	Fo’	qL	YNPQ	YNO
Supply Water	0.454 a	47.28 a	3.68 a	0.008 a	0.469 a	0.075 a
Fish Farming Effluent	0.431 a	36.26 b	4.22 a	0.009 a	0.483 a	0.085 a

Means followed by equal letters in the column do not differ by Student’s t-test at 0.05 probability.

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