The effect of application of effluent water on sage (Salvia officinalis L.) yield and quality in lysimeters

Implementation of water reclamation and reuse is a key factor in the pursuit of sustainable water resource management (Roccaro and Verlicchi, 2018). Wastewater reuse can satisfy different needs: irrigation requests, industrial purposes, potable demands and civil uses (Roccaro and Verlicchi, 2018). However, one of the major barriers according to the environmental aspects in implementation of wastewater reuse is salinity (Morris et al., 2021). The salinity of wastewater can come from a variety of sources, such as by-products from distilleries (Galbally et al., 2013), paper mills (Patterson et al., 2008; Quaye et al., 2011), wineries (Hirzel et al., 2017), agro-food, petroleum, textile and leather industries (Castillo-Carvajal et al., 2014; Pounsamy et al., 2019), tannery, drug and petrochemical industries (Srivastava et al., 2021), and even fish farming (Ibadzade et al., 2021; Kolozsvári et al., 2021). In spite of all these, agricultural waste water is used for irrigation in several countries (Qadir et al., 2010).

Agricultural irrigation using treated wastewater could promote both agriculture and water sustainability, but the primary focus of such a practice should be water recovery and its adoption locally (Ofori et al., 2021). The agricultural costs can be reduced by reusing wastewater for irrigation. This type of water can usually be put to use every season and has no access restrictions (Jiménez, 2006; Khater et al., 2015). Furthermore, severe water scarcity can be alleviated by the use of fish farming effluent water (Castro et al., 2006; Qadir et al., 2010; Soltani, 2017). Intensive fish farming and processing are characterised by the use of large amounts of water, thereby resulting in significant amounts of wastewater (de Melo Ribeiro and Naval, 2019). Water from fish farming has also been shown to be an effective nutrient supply (Haque et al., 2016). The combination of fish farming and agriculture can reduce the need for irrigation of fresh vegetable crops (McMurtry et al., 1997). In our previous research, we found that the effluent of an intensive fish farm in our town provides a constant amount of nutrient-rich water for irrigation, but its use is limited by its sodium and bicarbonate content (Kun et al., 2018a,b; Ibadzade et al., 2020; Kolozsvári et al., 2021). The goal of these experiments was to see if the effluent water from intensive catfish farming could be used to successfully grow herbs despite its salinity.

Saline water irrigation can cause secondary soil salinisation. However, water quality can be improved by the addition of gypsum, which can prevent the accumulation of sodium in the soil. According to the system of water quality classification of Richards (1954), for water characterised by a 0.25–0.75 dS · m⁻¹ EC and an 18–26 SAR value or a 0.75–2.25 dS · m⁻¹ EC and a 10–18 SAR value, a periodic soil improvement with gypsum is recommended (Richards, 1954; Vyas and Jethoo, 2015). In case of long-term irrigation using water with a high sodium content, it is recommended to dilute the water, if possible, and add Ca-containing materials (Simmons et al., 2009). In the experiments of Kun et al. (2018a), the addition of gypsum to diluted saline effluent water resulted in its improvement, to an extent that characterised it with a resemblance to good-quality river water; and it was classified into a better irrigation water category than the original effluent water according to the Hungarian classification, and the FAO and USDA classification systems as well (Kun et al., 2018a).

The use of saline water for irrigation on various crops, such as quinoa, okra, rice etc., has already been implemented (Azeem et al., 2020; Ibadzade et al., 2020; del Carmen Rodríguez-Hernández et al., 2021), but significantly less research has been done on the irrigation of medical herbs. Aktsoglou et al. (2021) assessed the effect of mild salinity stress during the soilless cultivation of fresh peppermint and spearmint in a floating system on biomass yield, product quality and plant secondary metabolite content. Ozturk et al. (2004) conducted studies to determine the effects of salt stress and water deficiency on some yield components and the essential oil content of lemon balm (Melissa officinalis L.). Omer et al. (2013) conducted a field experiment to study the effect of soil salinity and amino acids application on the vegetative growth, flower yield, chemical compositions and essential oil production of Matricaria recutita (L.). The research of Sabra et al. (2012) evaluated the physiological and biochemical responses of the three coneflower species Echinacea purpurea (L.) Moench, Echinacea pallida (Nutt.) Nutt. and Echinacea angustifolia (DC.) to NaCl salinity under hydroponic cultivation. Bistgani et al. (2019) aimed to evaluate the effects of saline irrigation, using different NaCl concentrations, on the growth, physiological characteristics, phenolic compounds and antioxidant activity of Thymus vulgaris and T. daenensis. Cordovilla et al. (2014) published the effect of salinity on thyme (T. vulgaris) and lavender (Lavandula angustifolia) plants, grown alone and in combination with each other.

The common sage (Salvia officinalis L.) is a drought and salt tolerant species and may be used in areas affected by these stresses. Salinity had no detrimental effects on these plants, up to a salinity level of 12.3 dS · m⁻¹ (Aslani and Razmjoo, 2018). Similar outcomes were reported by Kulak et al. (2020), who discovered that plant growth was not damaged until the attainment of a concentration of 150 mM, but that above this threshold, salinity adversely affected the development. However, many other studies in the literature completely contradict these results. Göçer et al. (2021) reported decreasing biomass parameters of two Salvia species with increasing EC level (salinity solution of NaCl with 1, 2, 3, 4, 5 and 6 dS · m⁻¹). Ben Taarit et al. (2009) also observed a decreased growth (63%) both in the shoot and the root at the above-mentioned threshold (100 mM). Hendawy and Khalid (2005) also found that plant height (PH), as well as fresh and dry leaves’ yield, decreased at the salinity level of 2,500 ppm. Moreover, 3,000 ppm sodium chloride was lethal for sage plants. This salinity level is equal with 50 mM sodium chloride. However, this is not an abnormal result, because the adverse effects caused by a level of salinity in excess of the tolerance range of the plant are well-documented in the literature, with multiple studies, delving into the salt effect on the growth of medical plants in particular, agreeing that there is a resultant inhibition. According to Kulak et al. (2020), different salt compounds with increasing concentration affect the vegetative growth and yield of Salvia officinalis (L.). Se applied at a concentration of 10 ppm brought about the maximum dry yield in sage (first harvest, 3.72 g · plant⁻¹), and additional Se reduced the influence of salt stress (Yaldiz and Camlica, 2021). MgCl₂ had a positive influence on dry herb yield, while the most detrimental effect was observed corresponding to the application of Na₂SO₄. Salt stress significantly affected the chemical composition of leaf essential oil in common sage, too, as demonstrated in the research of Es-sbihi et al. (2021), where a decrease in the essential oil content from 1.2% (control) to 0.4% (NaCl) was observed.

Beside the salinity effects, other environmental factors/stresses such as temperature, humidity, light intensity, supply of water and minerals can influence the amounts of oil components (Akula and Ravishankar, 2011; Verma and Shukla, 2015). Among the macronutrients, nitrogen (Rioba et al., 2015) and phosphorus (Nell et al., 2009) did not affect the content of the total essential oil in sage. However, in some components, the essential oil concentration increased with increasing N level (β-pinene) and the N × P interaction also affected α- and β-thujone accumulation (Rioba et al., 2015). Besides, the climate of the cultivation area and the time of harvest are also important factors in determination of the quantity and quality of essential oil content (Zheljazkov et al., 2012; Hassiotis et al., 2014). Traykova et al. (2019) reported that the application of hydroponic and aeroponic growing systems shortened the period from germination to harvest, enhanced plants’ flowering and reflected on the composition of the essential oil. The seasonal variation on the essential oil content was certified by Détár et al. (2020) and Gouvea et al. (2012).

The nitrogen content of sage shoot increased from 2.37% to 2.80% by the addition of 150 kg · ha⁻¹ nitrogen and 10 tons · ha⁻¹ zeolite. The maximum fresh (13,226.2 kg · ha⁻¹) and dry shoot (3,309.2 kg · ha⁻¹) weights were also measured in the treatment of 150 kg N · ha⁻¹ and 10 tons · ha⁻¹ zeolite, respectively (Hazrati et al., 2022). Salinity stress can cause nutrient deficiencies or imbalances due to the competitions between Na⁺ and K⁺ as well as Cl⁻ and NO₃⁻. These nutrient disturbances have a negative effect on plant growth and may change the macronutrients and sodium level of plants (Said-Al Ahl and Omer, 2011).

In our study, three irrigation treatments (with different water qualities) were applied during 2 consecutive years. We monitored the plant physiological parameters, the concentrations of sodium and main macronutrients of leaves, and total essential oil content as well as its composition. The experiment aimed to ascertain the applicability of effluent water irrigation to sage (Salvia officinalis L.) production, to determine the level of sodium uptake in leaves and to identify the effect of salinity on the oil composition and its stability.

Our experiment was carried out at the Lysimeter Station of the Research Center for Irrigation and Water Management (ÖVKI), Institute of Environmental Sciences, Hungarian University of Agriculture and Life Sciences (MATE), in Szarvas, Hungary. The soil type characterising the experimental site was Vertisol (Michéli et al., 2015; Schad, 2016). The soil properties that determine the capability of soils to deliver nutrients are shown in Table 1. Soil samples were taken from soil depths of 0–30 cm and 30–60 cm.

Meteorological characteristics

The experimental area is located in the temperate climatic zone with some Mediterranean effects and usually characterised by high fluctuations of temperatures and extreme water conditions (droughts, floods). The meteorological data for the specific growing seasons were provided by an Agromet Solar automatic meteorological station (Boreas Ltd., Érd, Hungary). These detailed meteorological parameters are described in Figure 1.

Figure 1.

In 2020, the total yearly precipitation (456.7 mm) was 60.0 mm more than the average for the years 1981–2010; and the average temperature was also higher, with a difference of more than 1°C. In 2021, the precipitation (328.9 mm) was 67.8 mm less than the average for 1981–2010, but the average temperature was 1°C higher. Comparing the experimental data across the various seasons, our results indicated that the precipitation was 127.8 mm more and the average temperature was 0.27 °C higher in 2020 than in 2021. The spring of 2021 (from March to May) was wetter and cooler (sum of precipitation, 137.9 mm; average temperature, 9.94 °C) than the spring of 2020 (103.3 mm and 11.18 °C, respectively). The precipitation fall for June 2020 was 123.8 mm, whereas June 2021 was extremely dry with only 1.2 mm of rainfall.

The effluent or reclaimed wastewaters are usually rich in salts (NaCl) and ammonia (Aloui et al., 2009). Accordingly, in our experiment also, the effluent water from the local fish farm was rich in bicarbonate, sodium and ammonia. However, it is characterised by low amounts of other nutrients (Table 2). Usually, aquaculture activities generate wastewater with high quantities of salts (31.1 ± 15 g · L⁻¹) (Srivastava et al., 2021). In our experiment, the sodium content of effluent water was about 276–282 mg · L ⁻¹ (12 mM), and this is much lower than the amount (830.30 mg · L⁻¹) reported by Castro et al. (2006). Rather, the sodium content observed in the present study aligns to a greater extent with those reported for the water studied by Karimov (2018) and Yeager et al. (2010).

Environmental factors are extremely important in the biosynthesis and accumulation of secondary metabolites (Akula and Ravishankar, 2011; Verma and Shukla, 2015). In terms of salt tolerance of sage, the sodium concentration of effluent water is not a relevant quantity, even if it was irrigated at a level of 105 mm in our experiment. The lethal dose of sodium for the sage plant is about 3,000 ppm in soil (Hendawy and Khalid, 2005). Al-Tabbal et al. (2016) used reverse osmosis (RO) rejected water with an extremely high (1,300 mg · L⁻¹) Na content for sage irrigation. They found that RO rejected water reduced the PH, the number of branches per plant, shoot fresh weight, shoot dry weight and root dry weight by 66%, 79%, 94%, 95% and 85%, respectively, compared to the control irrigation (Al-Tabbal et al., 2016). In the study of Aziz et al. (2013), even the application of 1.7 dS · m⁻¹ of NaCl caused 39.91% reductions of sage plant dry biomass in the second cut. When the NaCl concentration was 4.7 dS · m⁻¹, a 137.17% decrease was observed compared to the control (Aziz et al., 2013). Contrastingly, Aslani and Razmjoo (2018) reported no detrimental effects on plants up to a 12.3 dS · m⁻¹ salinity level. In our experiment, there was a similarity between the effluent water irrigation’s effectiveness on sage biomass production and that of the Körös-oxbow lake water irrigation. This result confirms the conclusion arrived at in the study of Ben Taarit et al. (2009), who did not detect yield decrease until a 25 mmol NaCl concentration.

Hendawy and Khalid (2005) proved that an increasing soil salinity (0–500–1,000–1,500–2,000–2,500 ppm) decreased the fresh and dry flowering herb yields by about 50%. Our results were higher (Table 5) than those of Hendawy and Khalid (2005), because the soil salinity in the present study was only 277.17 ppm corresponding to a soil depth of 0–30 cm, and the sodium content of our irrigation water was also lower with a high total nitrogen content (Table 2). According to Kulak et al. (2020) opinion, treatments under a 150 mM NaCl content do not cause yield damages. We applied irrigation water with a maximum NaCl content of 12 mM, and thus it was favourable for yield (Figure 2 and Table 5). Yaldiz and Camlica (2021) reported that the maximum dry yield of sage was measured from the first harvest (3.72 g · plant⁻¹). Contrastingly, Hendawy and Khalid (2005) reported that the second harvest gave the maximum yield. Our results showed that the September harvests resulted in the maximum yields in both the experimental years (dry leaves’ weight: 2020: Irr1, 67.98 ± 17.40 g · plant⁻¹; Irr2, 55.77 ± 18.23 g · plant⁻¹; and Irr3, 46.83 ± 9.47 g · plant⁻¹; 2021: Irr1, 40.34 ± 12.27 g · plant⁻¹; Irr2, 32.68 ± 7.52 g · plant⁻¹; and Irr3, 32.63 ± 4.90 g · plant⁻¹). According to Hazrati et al. (2022), treatment involving the addition of 150 kg N · ha⁻¹ + 10 tons · ha⁻¹ zeolite resulted in the maximum fresh shoot weight of 1.32 kg · m⁻². Our results (Table 9) indicate that we could reach a higher biomass production than Hazrati et al. (2022) with all irrigation treatments. Under control conditions, the Na content of sage leaf was 199.00–374.80 mg · kg⁻¹. This concentration is much lower than that (480 mg · kg⁻¹) involved in the study of Es-sbihi et al. (2021). Under salinity stress, we measured a Na content of 499.75 ± 42.79 mg · kg⁻¹ in 2020, and 430.50 ± 29.29 mg · kg⁻¹ in 2021. Besides stronger salinity stress, Es-sbihi et al. (2021) mentioned a 1,800 mg · kg⁻¹ sodium content; nevertheless, at a lower stress level (170 ppm sodium), Lorente et al. (2022) reported much lower Na⁺ concentration. The relationship between essential oil content and salinity stress is not unequivocal. The basic process is the same in many Lamiaceae plants as in glycophyta plants, in that salinity reduces the essential oil yield (Greenway and Munns, 1980). Contrastingly, notable changes in essential oil composition are not induced at low levels of salinity stress (Ben Taarit et al., 2009). Up to 2,500 ppm, an increasing Na⁺ concentration in the soil culture increased the oil content (Hendawy and Khalid, 2005). However, Es-sbihi et al. (2021) also confirm that the salt stress decreases the essential oil content. They reported a 33% decrease under 150 mM treatment compared to the control. Our result suggested that irrigation with effluent water decreased the total oil content in the average of 2 years (Irr1, 1.46 mL · 100 g⁻¹ d.m.; Irr2, 1.64 mL · 100 g⁻¹ d.m.; and Irr3, 1.75 mL · 100 g⁻¹ d.m.; Figure 3), especially in 2021 when the precipitation was much lower than in average seasons. This result also highlighted the importance of precipitation as an environmental factor. Missing precipitation causes water shortage, which triggers drought stress easily. Therefore, irrigation is of paramount importance. Mameli et al. (2011) also detected that the amount of irrigation has a significant effect on the oil content of sage. Moreover, it has been discovered that not only the irrigation amount but also the frequency of irrigation has a significant effect on the oil content of sage (Rioba et al., 2015). Plants generally produce higher levels of secondary metabolites under slight drought stress (Selmar and Kleinwächter, 2013). Similarly, Soltanbeigi et al. (2021) observed the highest essential oil content of sage (1.48%) after moderate drought stress. Moreover, additional fertilisers could increase the essential oil content even under serious water shortage compared to the optimal irrigation with NPK application (Soltanbeigi et al., 2021). Nahed et al. (2012) did not detect a significant difference between 80% of effectively irrigated sage plants and the control. However, Nowak et al. (2010) founded an elevated oil content already at 70% of the optimal water supply. The results arrived at in the study of Sonmez and Bayram (2017) also support the proposition that the highest essential oil content is produced corresponding to the prevalence of hot, dry seasons before harvesting.

The relative composition of essential oils varies remarkably with geographical position, climate conditions and several other factors (Şanli and Karadoğan, 2017). Our results are similar to those of Kulak et al. (2020), who indicated that the main components are a-thujone (26.13%–30.37%), camphor (21.90%–24.033%), ß-thujone (7.94%–10.93%), 1,8-cineol (syn: eucalyptol, 7.72%–9.78%) and ledol (5.83%–6.77%). Sonmez and Bayram (2017) detected α-thujone and ß-thujone; Es-sbihi et al. (2021) 1,8-cineol, α-thujone and camphor; and Ben Taarit et al. (2009) viridiflorol, 1,8-cineol, α-thujone and camphor as the main components. On the other hand, according to Aziz et al. (2013), the main components of essential oil of sage are α-thujone (17.28%–21.02%), cisthujone (8.68%–12.64%), camphor (13.45%–18.12%) and 1,8-cineole (7.21%–9.44%). The study of Aziz et al. (2013) demonstrated the highest essential oil percentage and yield vis-à-vis the highest NaCl (4.7 dS · m-¹) treatment in comparison with the control plants. We measured a lesser total content of essential oils in the treated plants in 2021, which indicates that the salinity in the effluent water had a stronger influence on oil content, besides the lower precipitation amount. However, significant differences in the main compounds of sage oil were not detected among the treatments. Despite the lower availability of water in the second year (2021), and although there were differences in terms of seasonal variation as well as different water qualities (Figure 4), the oil composition was strongly stable (Table 6). Aziz et al. (2013) found increasing percentages of the major components corresponding to increasing salinity levels, although a decrease in 1,8-cineole was one major observation, too (Aziz et al., 2013).

Effluent and gypsum-supplemented effluent water irrigation provide good opportunities to conserve fresh water resources, because the response, especially in terms of the resultant essential oil content, elicited in the sage plant to these methods is similar to that observed corresponding to surface water irrigation. The applied water quality had a significant impact only on the following components, namely camphene, trans-sabinole and caryophyllene-oxide. However, the total essential oil yield was reduced in Irr1 in the second experimental year, compared with the effluent water from intensive catfish farm treatment and Körös-oxbow water irrigation. In consideration of these effects, we can conclude that the effluent water from the African intensive catfish farm, as well as similar effluent water subject to dilution, can be applied towards the irrigated cultivation of sage.