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.
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 (AN), stomatal conductance (gs), and transpiration (E) of the seedlings with increasing NPK fertilization. An important fact is that the AN 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 AN 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 (YNPQ), and non-regulated quantum yield of photochemical quenching (YNO) 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 (
YNPQ) and minimize the loss of energy through kinetic and resonance processes in PSII (
YNO) [
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 (H
2O) m
−2 s
−1, a decrease in transpiration from 0.70 to 0.45 mmol (H
2O) m
−2 s
−1, a decrease in photosynthesis from 4.02 to 1.10 µmol (CO
2) 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 (H
2O) m
−2 s
−1 and a mean value of transpiration of 1.67 mmol (H
2O) m
−2 s
−1. The photosynthetic rate had a mean value of 3.90 µmol (CO
2) 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.