Cattle manure and bio-nourishing royal jelly as alternatives to chemical fertilizers: Potential for sustainable production of organic Hibiscus sabdariffa L.

Highlights

• Combining cattle manure (CMn) with reduced amounts of chemical fertilizers (CFs) + royal jelly (RJ) improved roselle growth.

• CMn + reduced amounts of CFs + RJ improved roselle sepal yield and quality.

• CMn + reduced amounts of CFs + RJ improved roselle nutrient status.

• CMn + reduced amounts of CFs + RJ improved antioxidant and phytohormone contents in roselle plants.

• Applying the CMn and RJ is the potential for sustainable production of organic roselle.

Abstract

For sustainable and organic farming, organic manures such as cattle manure (CMn) and bio-nutritious substances such as royal jelly (RJ) should be used as complete or at least partial alternatives to chemical fertilizers (CFs). Therefore, two consecutive trial seasons (2018 and 2019) were conducted to study the effect of soil fertilization with CMn and/or CFs in combination with foliar spraying with RJ on growth, yield, and chemical composition of roselle (Hibiscus sabdariffa L.) plant and seed. The results indicated that spraying roselle plants with RJ resulted in a significant increase in all parameters studied over the control; however, this increase was enhanced when RJ was combined with soil fertilization. The highest values for most of the growth traits, chemical composition of seeds, sepal anthocyanin and vitamin C contents, and sepal acidity were obtained by applying 2 or 4 g RJ L⁻¹ + (30 m³ CMn ha⁻¹ + 50 % dose CFs). In addition, the highest values for yield components and plant chemical composition were obtained by applying 2 or 4 g RJ L⁻¹ + (0 m³ CMn ha⁻¹ + full dose CFs). The results also indicated that applying CMn in combination with RJ gave values mostly close to those of CFs treatment. In conclusion, the results recommend the use of RJ (2 g L⁻¹ as a foliar feeding) along with CMn (30 m³ ha⁻¹) as a partial alternative to chemical fertilizers for sustainably producing healthy roselle sepals.

Introduction

Among the indigenous African crops, roselle (Hibiscus sabdariffa L.) is a nutritious plant that is consumed globally for its high value and entry to world markets (Sanders et al., 2020). It is a medicinal plant that belongs to the Malvaceae family. It is widely used as a food, along with the use of calyces, dried or fresh, in the preparation of hot, cold, and fermented herbal drinks and beverages, wine, jam, jelly, ice cream, chocolate, flavoring agents, puddings, and cakes. It is also used in the pharmaceutical and cosmetic industries using its oil (Ismail et al., 2008; Bolade et al., 2009). In traditional medicine in India, Africa, and Mexico, infusions from calyces or leaves are used to treat fever, liver disease, hypertension, hypercholesterolemia, gastrointestinal disorders, and as a diuretic (Monroy-Ortiz and Castillo-Espana, 2007) or to help reduce elevated body temperature as in Egypt and Sudan (Leung and Foster, 1996). Extracts from its calyces have anticancer (Olvera-García et al., 2008) and antioxidant property (Ramakrishna et al., 2008). All these properties are attributed to the rich nutritional formula of Hibiscus sabdariffa. This plant is of obvious importance from a nutritional and medicinal point of view. Its calyces, leaves, and seeds are rich in organic acids, minerals, amino acids, carotene, vitamin C, sugars, flavonoids, anthocyanins, triterpenoids, steroids, and alkaloids at variable levels according to variety and geographical area. Besides, the seeds are a valuable food source due to their high protein, calorie, fibers, and micro-nutrient contents (Mady et al., 2009).

Chemical fertilizers (CFs) are necessary for the amount of agricultural yield, as they are used to obtain an increase in crop production (Moncayo and Dreyer, 2018) to achieve food security for the world population (Kiran et al., 2016). In contrast, there may be also some side effects due to non-professional applications. Intensive and unbalanced use of CFs in the long term decreases soil base saturation and acidification (De-Ridder and Van-Keulen, 1990). CFs cause several deleterious effects on the environment and human health (Yeshiwas et al., 2018). They increase soil degradation, pH, heavy metal accumulation, and underground water pollution, leading to reduced soil fertility (Agbo et al., 2012; Soro et al., 2015) and may cause heavy metals accumulation in plant tissues, thus negatively affecting the crop nutritional value and edibility (Shimbo et al., 2001). As a result, there has been a trend towards the use of fertilizers from natural sources, which can provide renewable and organic sources of nutrients for crops (Roe, 1998; Kurt and Ayan, 2013; Kahil et al., 2017) to return to rebalancing the troubled ecological balance (due to improper practices of an organic sustainable agro-ecosystem) using conscious farming techniques and natural approaches (Tasbasli et al., 2003).

For food safety, harmful effects on the environment must be minimized by increasing the nutritional properties of organic products (Zaccone et al., 2010) applied to soils, as well as obtaining healthy foods and products (Ekelund and Tjärnemo, 2004). This will result from a significant improvement in soil structure and stability, higher yields, and especially crop quality (Chang et al., 2010; Marzouk and Kassem, 2011) as the main challenge behind the implementation of the organic farming system. However, organic manure (OMn) such as CMn should not be used at excessive levels in order not to cause nitrate (NO₃⁻) build-up in the soil and become a potential pollutant in the ground or surface water, which delays fruiting and increases the risk of disease, freezing, and wind damage (Bary et al., 2004). To bypass such an issue, testing soil and CMn nutrient contents can help determine the appropriate needs and amount of CMn required.

As an animal waste, CMn has been used to preserve soil fertility for centuries (Castrillón et al., 2002). It is a mixture of faeces, manure, bedding material, wasted feed, and water. CMn contains most of the nutrients needed for plant growth. It has a high percentage of organic matter (OMt) and can replace or reduce the need for CFs in crop production. However, the nutrient concentration of CMn is very low, and they are present in the organic and inorganic forms. Therefore, large application rates are required to provide equivalent nutrient intake. Solid CMn is high in nutrients in the non-plant available organic fraction. The organic form of the nutrient must be mineralized to convert it to the inorganic form. Solid CMn usually contains 10–20 % of N readily available in the inorganic fraction. The availability of P in CMn is estimated to be about 50 % compared to commercial P fertilizer and the response to P depends on the availability of other nutrients in the manure such as N (SSCA, 2000).

Royal jelly (RJ), a powerful novel nutrient that was used in this study for hibiscus plants as foliar nutrition, is an effective strategy to enrich the organic farming system. RJ is produced from the hypopharyngeal, mandibular, and post cerebral glands of a young worker bee nurse (bees 5–14 days old) (Fujita et al., 2013). It has a yellowish-white color, a gelatinous-viscous sour taste, with a slight characteristic odor of phenol (which gives it a distinct odor) (Fratinia et al., 2016), and relatively acid (pH 3.6–4.2) (Seven et al., 2014; Fratinia et al., 2016). It is rich in vitamins, proteins, enzymes, fatty acids, peptides, and flavonoids (Tokunaga et al., 2004; Melliou and Chinou, 2005; Vucevic et al., 2007). Hence, the intellectual property of RJ has been adopted since ancient times in folk medicine, especially in Asian apitherapy, but also in ancient Egypt. Nowadays, it is used in pharmaceutical and cosmetic fields, and it is marketed as a functional food without a prescription (Cornara et al., 2017). Various studies have reported on RJ's antioxidant properties, due to phenols and polyphenols, in major protein structures. In addition to stimulating growth, prevention of infection, anti-hypercholesterolemia, anti-inflammatory activities, and immunostimulating effects (Nagai and Inoue, 2004; Guo et al., 2008; Viuda-Martos et al., 2008; Pavel et al., 2011).

Although RJ has rarely been applied in a few studies to increase plant growth, chemical constituents, and production (El-Shaikh, 2010; Abada and Ahmed, 2015; Nassef and El-Aref, 2016), this is the first time that we have attempted to use it as an alternative organic source for leafy plant nutrition to qualify it to incorporate organic farming systems. As RJ possesses the key ingredients that make it a valuable biostimulant and bio-nutritive, it can be used in combination with CMn as an alternative to chemical fertilizers for the potential to sustainably produce organic roselle. Therefore, this study aimed to evaluate the effect of foliar feeding with RJ as an alternative to CFs in integration with soil supplementation with CFs and/or CMn on morphological and yield traits, nutrient homeostasis, photosynthetic efficiency, endogenous phytohormones, and antioxidants (enzymatic and non-enzymatic) activities of roselle plants. In addition, to compare these obtained parameters with plant fed chemically with those obtained with plants fed organically.