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Article

Shrimp-Waste-Derived Biochar Induces Metal Toxicity Tolerance of Wastewater-Irrigated Quinoa (Chenopodium quinoa)

by
Magdi A. A. Mousa
1,*,
Kamal A. M. Abo-Elyousr
1,
Omer H. M. Ibrahim
1,
Nouf Owdah Alshareef
2 and
Mamdouh A. Eissa
3
1
Department of Arid Land Agriculture, Faculty of Meteorology, Environment and Arid Land Agriculture, King Abdulaziz University, Jeddah 80208, Saudi Arabia
2
Department of Biochemistry, Faculty of Science, King Abdulaziz University, Jeddah 80208, Saudi Arabia
3
Department of Soils and Water, Faculty of Agriculture, Assiut University, Assiut 71526, Egypt
*
Author to whom correspondence should be addressed.
Agriculture 2022, 12(11), 1748; https://doi.org/10.3390/agriculture12111748
Submission received: 15 September 2022 / Revised: 20 October 2022 / Accepted: 21 October 2022 / Published: 22 October 2022
(This article belongs to the Special Issue Crop Antioxidant System and Its Responses to Stress)
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Abstract

:
The scarcity of high-quality water resources may lead to the use of lower quality water for plant production. Quinoa (Chenopodium quinoa) plants have great potential for human nutrition, but poor water quality, such as metal contamination in wastewater, affects the seed quality. This study aims to investigate the effects of shrimp-waste-derived biochar (SWB) on the uptake of toxic metals from wastewater by quinoa plants. Additionally, the study investigates how quinoa plants’ antioxidant defenses respond to wastewater and SWB treatments. Shrimp-waste-derived biochar (SWB) was prepared by pyrolysis at 350 °C for 3 h and added to the soil at the levels of 0, 1, and 2% (based on soil weight), which are namely C, SWB1, and SWB2, respectively. SWB was applied to quinoa plants cultivated in pots filled with sandy soil and irrigated with fresh or wastewater for a continuous 90 days. The wastewater was contaminated with manganese (Mn), iron (Fe), copper (Cu), zinc (Zn), cadmium (Cd), and lead (Pb). Quinoa seeds that were irrigated with wastewater had Cd and Pb concentrations that were above the allowable levels (for human consumption) in the absence of biochar (C) or addition of SWB1. Wastewater significantly reduced quinoa growth and photosynthetic pigments, while SWB significantly mitigated the metal toxicity and improved growth. SWB2 significantly reduced the Pb and Cd concentrations in quinoa leaves by 29 and 30% compared with C. The Cd and Pb concentrations in quinoa seeds were safe for human consumption and below the maximum allowable limits when the soil was amended with SWB2. SWB improved the synthesis of photosynthetic pigments and increased the activity of antioxidant enzymes such as polyphenol oxidase and ascorbate peroxidase. SWB reduced the toxic metal availability and uptake, mitigated the oxidative stress, and minimized the levels of malondialdehyde and hydrogen peroxide. The SWB addition stimulated quinoa’s antioxidant defense and protected plant cells by eliminating reactive oxygen species. The addition of 2% (w/w) shrimp waste biochar improved the quality of quinoa seeds irrigated with wastewater and decreased their toxic metal content. The obtained results contribute to sustainable development and the exploitation of wastewater to irrigate quinoa plants in arid degraded soil; additionally, it also helps in the recycling of shrimp waste.

1. Introduction

Toxic metal contamination of soils and water is a major concern, causing stress and toxicity in plants and, ultimately, a loss in yield and food quality [1,2]. He et al. [3] reported that pollution with heavy metals may lead to losses in the global economy estimated at 10 billion dollars per year. Heavy metals are non-degradable in soil, fast-moving, highly toxic, and easily absorbed by plants; therefore, they are capable of causing damage to the growing crop, as they negatively affect the quality of the food produced from this crop [4,5]. Dealing with the problem of heavy metal pollution has become more urgent because of the rise in food demand brought on by population growth [1]. Lack of freshwater resources forces farmers in some parts of the world to irrigate crops with wastewater, which can contaminate the soil and introduce heavy metals into the food chain [5,6]. It is necessary to study the crop’s resistance to contamination with heavy metals and the places where these elements gather in plant tissues to know the extent of the danger to human health [5,7]. Reactive oxygen species (ROS) appear under metal stress, causing a harmful effect on plant cells and a reduction on plant growth [8]. Different defense mechanisms are used by plants to protect themselves from ROS [8]. The antioxidant system in plants is one of the most important ways that plants use to reduce the negative effects of ROS in in their cells [9]. Enzymatic and non-enzymatic compounds are the two major systems that make up the antioxidant defense [8,10]. Plant cells secrete many antioxidant enzymes such as ascorbate peroxidase, pyrogallol peroxidase, and polyphenol oxidase, whereas non-enzymatic antioxidants include phenolic compounds, glutathione, proline, and soluble carbohydrates [9]. The cultivation of halophytes e. g., quinoa plants in saline soils and using wastewaters may be considered as the most suitable and promising approach to deal with food security [11,12].
Quinoa (Chenopodium quinoa Willd) can be a crop for food security because of its highly nutritious grains [12,13,14]. Quinoa plants have been cultivated in more than 120 countries; the top producers are Peru, Bolivia, Ecuador, the United States, Columbia, Chile, and Brazil [13]. Bolivia and Ecuador are the two largest quinoa producers in the world, with a cultivated area of 172,000 hectares [13]. Quinoa plants can also be successfully grown in saline water and can withstand drought stress [12,13,14]. The seeds of quinoa plants have highly nutritional values even if cultivated in harsh environment, as in the case of irrigation with wastewater and contaminated soils [12,14]. It is unclear how heavy metals are absorbed by wastewater-irrigated quinoa and how metal stress tolerance works.
The use of soil amendments, such as biochar, to immobilize metal from soil solution and to reduce metal uptake by plants has become increasingly popular recently [15,16,17]. It is possible to water plants with polluted water because biochar helps crops absorb fewer metals [15]. Biochar can reduce metal bioavailability through different mechanisms, thereby mitigating metal toxicity to plants and soil microorganisms [16,17]. Biochar is rich with organic compounds and has a high cation exchange capacity and surface area [17,18,19]. Organic compounds in biochar contain many functional groups, e.g., phenolic hydroxyl, carboxyl, carbonyl, and ester [17,18,19]. Heavy metals are immobilized in the soil solution by the functional groups of biochar, which serve as a bridge between metals and biochar [17,20]. The outstanding physical and chemical properties of biochar, such as large surface area and high cation exchange capacity, enable it to decrease the mobility of heavy metals in soil and thus reduce their absorption by plant roots [17,21]. Biochar may help to increase the ability of plants to tolerate metal stress by reducing metal availability in soil and improving soil fertility, physicochemical priorities, biochemical functions, and soil enzymes activities [16,22]. Shrimp waste is high in valuable organic material that has the potential to be used as a soil amendment [23]. The wastes of shrimp in the form of skin and head represent 40–50% of the shrimp weight, and these huge amounts of waste must be recycled [23]. The highly valuable compounds that can be recovered from shrimp waste allow it to be used as a soil amendment in the cultivation of vegetables and field crops [24]. The outstanding chemical composition and high nutrient content of shrimp waste increase its ability to improve plant growth and nutrient uptake [23]. Shrimp waste contains 42, 17, 29, and 5% (w/w) protein, chitin, ash, and fat, respectively [25]. The organic compounds in shrimp waste have several active sites that can absorb heavy metals, forming ion exchange or chelating mechanisms, consequently reducing the metal bioavailability [26,27].
The soils present in arid regions have low organic matter content, and the risk of heavy metal absorption by plants increases when polluted water is used for irrigation [5]. Our hypothesis is that when quinoa plants are irrigated with metal-contaminated water, the addition of biochar derived from shrimp waste will lessen the availability and uptake of toxic elements. Therefore, this study aims to explore and understand the role of biochar created from shrimp waste that is rich with organic matter and calcium in reducing the transfer of toxic elements from wastewater to quinoa plants grown in arid degraded soils.

2. Material and Methods

2.1. Biochar Production and Characterization

The wastes of shrimp were brought from a fish restaurant located in Assiut Governorate, Egypt. The collected waste was air-dried and crushed. Shrimp waste was pyrolyzed at 350 °C for 3 h before being crushed and sieved through a 2 mm sieve. The loss-on-ignition method described by Matthiesen et al. [28] was used in the determination of the total organic carbon of the biochar sample. Biochar pH was determined in 1:5 (biochar/water) by a digital pH meter. Biochar salinity was measured by an electrical conductivity meter [29]. The biochar sample was digested by a mixture of HClO4 and HNO3 at a ratio of 1:2 [30]. The concentrations of potassium (K), calcium (Ca), iron (Fe), manganese (Mn), zinc (Zn), copper (Cu), lead (Pb), and cadmium (Cd) in the digested biochar sample were determined by ICP−OES, thermo iCAP 6000 series. The detection limits for Cd and Pb are: 0.07 and 1.06 µg L−1, respectively. Nitogen (N) in the biochar sample was determined by the Kjeldahl method, while phosphorus was determined by a spectrophotometer at 660 nm. Table 1 shows the main characteristics of shrimp waste biochar (SWB). The surface morphology of the shrimp waste biochar was examined by scanning electron microscopy (SEM) using a Carl Zeiss sigma 500 VP and JSM 5400 LV. The SEM image of shrimp waste biochar is shown in Figure 1. The electron micrograph of the biochar sample shows that it has a sheet structure and is characterized by a large specific surface area.

2.2. Soil Characterization and Pot Experiment

A soil sample was collected from the tillage layer (0–20 cm) of a private farm in Assiut Governorate, Egypt and sieved with a 2 mm sieve, and then packed into pots with a capacity of 5 kg. The soil is classified as Arenosols according to FAO/WRB [31]. The soil texture was determined by hydrometer method as described in Burt [29]. The soil pH was measured in a 1:2 soil to water ratio based on the method of Burt [29]. The available forms of Fe, Mn, Zn, Cd, Pb, and Cu in the studied soil were extracted by 0.005 M DTPA [32] and then determined by ICP−OES. The soil organic carbon was measured by the dichromate oxidation method [29]. The concentrations of soil available nitrogen, phosphorus, and potassium were determined according to Burt [29]. The same methods of soil analysis were used in the determination of soil properties at the end of the pot experiment. Table 2 shows the basic soil characteristics of the soil under study.
Shrimp-waste-derived biochar (SWB) was mixed with the studied soil and filled in the pots before the cultivation of quinoa (Chenopodium quinoa cv. Utosaya Q37). SWB rates were 0, 1, and 2% (w/w) (C, SWB1, and SWB2, respectively). Each treatment was replicated five times. Four seeds of quinoa were sown in each pot and then thinned to two plants after full germination. Quinoa plants were amended with nitrogen (1 g/pot) in the form of urea (46% N) after 20 and 50 days from sowing, respectively. Two types of water were used in the irrigation of quinoa plants, and Table 3 shows the main properties of the tested waters. The freshwater was tap water, while the wastewater was brought from the wastewater treatment plant in Assiut, Egypt. The properties of fresh and wastewater were determined using the standard methods described in the soil analysis section. During the experiment period, the soil moisture was kept near field capacity via the daily addition of evaporated water. The experiment was conducted in open climatic conditions (solar radiation of 25–30 MJ/m2/day, relative humidity of 50–60%, and temperature of 20–25 and 10–14 °C, respectively, for Tmax and Tmin). After 90 days from sowing, the plants were harvested, and then the plant height and fresh weight per pot were recorded. After being cleaned with distilled water and dried in an oven at 70 °C, the harvested plants’ total dry matter weight was recorded.

2.3. Plant Analysis

The plant samples were digested with a mixture of H2SO4 and H2O2, as described by Parkinson and Allen [33]. The photosynthetic pigments, i.e., total chlorophyll and carotenoid contents, were extracted by ethyl alcohol (95%) [34]. The extracted pigments were measured by spectrophotometry at 663, 644, and 452 nm, respectively [34]. Oxidative stress was monitored by determining stress markers such as hydrogen peroxide (H2O2) using the method of Wohlgemuth et al. [35] and Rodríguez-Serrano et al. [36]. Lipid peroxidation assessed as malondialdehyde (MDA) content was quantified using the method of Madhava and Sresty [37]. According to Madhava and Sresty [37], MDA was quantified using the thiobarbituric acid method and then calculated from the absorbance using 532 nm at a spectrophotometer. The method developed by Chen and Asada [38] was used to measure the activity of ascorbate peroxidase (APO) and polyphenol oxidase (PPO). Ascorbic acid, potassium phosphate, hydrogen peroxide, and enzyme extract make up the determination’s reagents.

2.4. Data Analysis

The trial studied two factors (2 water types × 3 biochar doses) and consisted of 6 different treatments. To determine whether differences between the investigated treatments were significant, a one-way analysis of variance (ANOVA) was conducted, and Duncan multiple range tests were used to compare the means. All the statistical analyses were run by the SPSS 17.0 software package (SPSS, Chicago, IL, USA).

3. Results

3.1. Heavy Metals and Soil Quality Characteristics

The addition of shrimp-waste-derived biochar (SWB) caused remarkable effects on the studied soil attributes and metal bioavailability (Table 4). SWB significantly increased the soil pH and soil organic carbon. The application of SWB1 increased the soil organic carbon by 9 and 19%, respectively, in the case of fresh and wastewater, while these increases were 9 and 23% in the case of SWB2. The irrigation of the sandy soil with wastewater significantly increased the availability of Fe, Mn, Zn, Cu, Pb, and Cd, while the biochar addition significantly minimized the metals availability. SWB1 reduced the availability of Fe, Mn, Zn, Cu, Pb, and Cd by 21, 8, 16, 9, 28, and 16%, respectively, in the wastewater irrigated soil. The addition of the high level of biochar (SWB2) was more effective than SWB1 in minimizing the metal availability in the wastewater-irrigated soil. SWB2 minimized the availability of Fe, Mn, Zn, Cu, Pb, and Cd by 22, 19, 26, 12, 34, and 28%, respectively, in the case of waste-irrigated soil.
The availability of nitrogen (N), phosphorus (P), potassium (K), and calcium (Ca) in soil was significantly increased by the addition of SWB1 and SWB2 (Table 5). The wastewater-irrigated soil that received the highest rate of shrimp waste biochar 2% (w/w) was found to have the highest significant value of nutrient availability.

3.2. Nutrient Uptake, Photosynthetic Pigments, and Quinoa Growth

N, P, K, and Ca concentrations in the quinoa shoot significantly increased after the addition of SWB1 and SWB2 (Table 6). The maximum significant value of nutrient uptake was found in the wastewater-irrigated soil that received the highest rate of shrimp waste biochar.
Wastewater significantly minimized the synthesis of photosynthetic pigments, on the other hand, the application of SWB significantly enhanced the synthesis of photosynthetic pigments (Figure 2A,B). The irrigation of quinoa plants with wastewater reduced the total chlorophyll and carotenoids by 27 and 12% in comparison with freshwater. The application of SWB1 increased the total chlorophyll and carotenoids by 38 and 49% in the case of freshwater, while these increments were 61, 29, 42, and 50% in the case of wastewater. SWB2 addition increased the total chlorophyll and carotenoids by 44 and 57% in the case of freshwater, while these increments were 67 and 90% in the case of wastewater.
Wastewater significantly reduced quinoa growth parameters compared with freshwater, while the application of SWB significantly mitigated the toxicity of wastewater (Figure 3A–C). The irrigation of quinoa plants with wastewater significantly reduced the plant height (PH), fresh weight (FW), and dry weight (DW) by 16, 10, and 13%. SWB significantly improved quinoa growth parameters, and the highest rate (SWB2) was more effective than SWB1. SWB1 addition increased PH, FW, and DW by 10, 8, and 18% in the case of freshwater, while these increments were 13, 3, and 13% in the case of wastewater. The growth parameters, i.e., PH, FW, and DW, were increased by 20, 12, and 35% when the soil was amended with SWB2 in the case of freshwater, while these increments were 33, 10, and 33% in the case of wastewater.

3.3. Metals Concentrations in Quinoa Leaves and Seeds

Iron (Fe), manganese (Mn), zinc (Zn), copper (Cu), lead (Pb), and cadmium (Cd) in the leaves of quinoa plants were affected significantly by the wastewater treatment (Figure 4A–F).
The leaves of quinoa plants that were irrigated with wastewater significantly contained higher concentrations of Fe, Mn, Cu, Zn, Cd, and Pb than those irrigated with freshwater. SWB addition significantly reduced the levels of Fe, Mn, Cu, Zn, Cd, and Pb in quinoa leaves compared with the non-amended soil (C). SWB1 reduced Fe, Mn, Zn, and Cu concentrations in quinoa leaves that were irrigated with wastewater by 7, 10, 12, and 15%, respectively, compared with C, while these reductions were 10, 13, 19, and 22% in the case of SWB2. The concentrations of Pb and Cd in quinoa leaves irrigated with freshwater were not noticeable, but they were very high in the plants irrigated with wastewater. Concentrations of Pb and Cd in the leaves of quinoa plants irrigated with wastewater ranged between 25–35 and 10–15 mg kg−1, respectively. The application of SWB1 and SWB2 significantly reduced the concentrations of Cd in quinoa irrigated with wastewater by 20 and 30% compared with C, while these reductions were 14 and 29% in the case of Pb (Figure 4E,F). The concentrations of the studied metals in the seeds of quinoa irrigated with wastewater were significantly higher than those irrigated with freshwater (Table 7). The concentrations of the studied metals were less than the maximum permissible values in the cases of Fe, Mn, Zn, and Cu. The addition of SWB significantly decreased the concentrations of Fe, Mn, Zn, Pb, and Cd in quinoa seeds. Quinoa seeds irrigated with wastewater contained concentrations of Cd and Pb higher than the permissible limits in the absence of biochar (C) or the addition of the low-level SWB1. The addition of SWB2 reduced Cd and Pb concentrations to levels below the maximum allowable limits.

3.4. Physiological Response of Quinoa Plants to Metal Toxicity and Biochar Addition

The irrigation of quinoa plants with wastewater significantly increased the activity of antioxidant enzymes, i.e., ascorbate peroxidase (APX) and polyphenol oxidase (PPO) (Figure 5A,B). Moreover, the wastewater increased the oxidative stress markers, i.e., malondialdehyde (MDA) and hydrogen peroxide (H2O2) (Figure 5C,D). Wastewater, in comparison with freshwater, caused 50, 104, 69, and 53% elevated levels of APX, PPO, MDA, and H2O2 in quinoa leaves. SWB increased the activity of antioxidant enzymes and mitigated the oxidative stress that resulted from metal toxicity. The application of SWB1 to the wastewater-irrigated quinoa increased APX and PPO by 13 and 20% and reduced MDA and H2O2 by 20 and 13% in comparison with the control (Figure 5A–D). The application of SWB2 to the wastewater-irrigated quinoa increased APX and PPO by 20 and 47% and reduced MDA and H2O2 by 50 and 25% in comparison with the control.

4. Discussion

Wastewater significantly reduced the growth of quinoa plants compared with freshwater. The reduction in quinoa growth may be due to the toxicity of heavy metals in the wastewater. The wastewater used in this study contained Mn, Cu, Cd, and Pb above the permissible limits according to the FAO [39] water guidelines. Although the wastewater caused significant increases in the levels of Fe, Zn, and Mn in the leaf tissues, the concentrations of the mentioned elements were less than the toxicity levels. Based on dry weight, the toxicity levels of Fe and Mn in plant tissues ranged from 400 to 1000 mg kg−1, while Zn was between 100 and 400 mg kg−1 [40]. The use of wastewater in the irrigation of quinoa plants increased the concentrations of Cu, Cd, and Pb in the leaves of quinoa plants above the toxicity levels. The toxicity level of Pb, Cu, and Cd in plant tissues ranged from 30 to 300, 20 to 100, and 5 to 30 mg kg−1 [40]. The presence of Pb, Cu, and Cd in toxic concentrations within the tissues of quinoa made the plant direct a large part of its energy to carry out vital processes that reduced the adverse effects of element toxicity, which consequently led to a reduction in quinoa growth [30]. Toxic metals, e.g., Cd, Pb, and Cu, inhibit some physiological processes and cause damage in cell membranes, and consequently minimize quinoa growth [21]. Increasing the levels of toxic metals in plant tissues deteriorates the plants defense system, causing several morphological and physiological disturbances, e.g., the activity of antioxidant enzymes, chlorophyll synthesis and photosynthesis processes, and imbalances in nutrients [41]. Wastewater caused a significant reduction in the concentrations of photosynthetic pigments in quinoa due to the toxicity of Cd, Pb, and Cu in the plant leaves [20,21]. Increasing the levels of toxic metals in the leaf tissue may lead to a distortion in the chloroplast, which causes a reduction in the synthesis of photosynthetic pigments [20,21,42]. SWB mitigated the negative effects of wastewater and significantly increased the photosynthetic pigment levels in quinoa plants. The addition of SWB enhanced the physiological attributes and improved the nutrient uptake by quinoa plants [43,44]. The biochar of shrimp waste significantly increased the synthesis of chlorophyll by raising the photosynthetic activity under metal toxicity [45,46].
The levels of toxic metals in the quinoa seeds increased when they were irrigated with wastewater. Similar results were found by Eissa and Negim [5]. According to the FAO/WHO [1], all the studied metals were less than the permissible values, except for the concentrations of Cd and Pb. Biochar addition significantly reduced the studied metals in quinoa seeds. The SWB addition augmented the resistance of quinoa plants to metal stress toxicity. SWB was successful in altering the soil’s characteristics to lower the bioavailability of heavy metals. It was clearly demonstrated that the ability of SWB to raise the soil pH and organic matter led to a reduction in the availability of the examined heavy metals. SWB has a high content of organic matter; in addition to that, most of the organic compounds are stable and resistant to decomposition by microbes [47]. The functional chemical groups, e.g., OH and COOH, in biochar fix the toxic metals mainly by surface complexation and ion exchange process [6,48]. Biochar application to the metal-polluted soils reduced the toxic metals availability [47,49]. Another mechanism that may have contributed to increasing the plant’s resistance to metal toxicity is that increasing soil organic matter plays a significant part in enhancing the plant’s uptake of nutrients [12]. Quinoa biomass clearly increased after biochar was mixed with wastewater-irrigated soil compared with unaltered soil. This improvement could be credited to biochar’s role in enhancing soil quality [12]. The production of phytohormones, altered soil microbial activity, and corrected nutrient uptake all contribute to SWB’s ability to accelerate quinoa growth [12,18].
The addition of SWB to the quinoa plants that were receiving wastewater irrigation increased the activity of antioxidant enzymes such as APX and PPO (Figure 6). The decrease in heavy metal content in the quinoa shoots brought on by the addition of SWB may account for the increase in antioxidant enzyme activities. Quinoa plants stimulated the activity of antioxidant enzymes to mitigate the oxidative stress caused by the heavy metal toxicity in the wastewater. The toxicity of heavy metals in the wastewater increased the MDA and H2O2 concentrations in quinoa plants due to the oxidative stress caused by the heavy metals [50,51].
The addition of SWB mitigated oxidative stress and significantly reduced the MDA and H2O2 levels in quinoa plants by reducing the levels of heavy metals in the plant tissues. The addition of biochar reduced the oxidative stress in wheat and spinach plants [52,53]. We hypothesize that SWB addition improved the antioxidant defense that eliminates reactive oxygen species, especially H2O2, and protected the cells of quinoa plants. This hypothesis is supported by the study’s findings, which showed that adding biochar significantly improved the production of chlorophyll and the activity of antioxidant enzymes, which were linked to lower levels of reactive oxygen species, e.g., H2O2. Abbas et al. [52] and Shahbaz et al. [54] have shown that adding biochar to plants grown in metal-toxic environments improves the activity of antioxidant enzymes. The mechanism of biochar action in improving plant antioxidant defense systems may be due to its ability to scavenge ROS and improve plant health by dropping the concentrations of toxic metals in plants [55,56].

5. Conclusions

Agricultural expansion in crop production using limited water resources and arid degraded soils represents a great opportunity to supply food to the growing global population in our world. The addition of shrimp-waste-derived biochar (SWB) to wastewater-irrigated quinoa plants improves growth and enhances metal toxicity tolerance. SWB is rich in organic compounds that help in the control of heavy metals in wastewater and minimize their transfer to quinoa grown in degraded soil that suffers from low organic matter. The addition of SWB contributes to reducing the transfer of heavy metals to the food chain when irrigating plants with low-quality water. The results obtained provide an opportunity for agricultural expansion in arid regions, as well as the use of wastewater. Field studies are required to determine the impact of adding shrimp waste on the soil and plant environment, particularly when using a wastewater irrigation system.

Author Contributions

Conceptualization M.A.A.M., K.A.M.A.-E., O.H.M.I., N.O.A. and M.A.E.; methodology M.A.A.M., K.A.M.A.-E., O.H.M.I., N.O.A. and M.A.E.; software, M.A.E.; validation, M.A.E. and K.A.M.A.-E.; data curation, M.A.E. and O.H.M.I.; writing—original draft preparation, M.A.A.M., K.A.M.A.-E., O.H.M.I., N.O.A. and M.A.E.; writing—review and editing. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Deputyship for Research & Innovation, Ministry of Education in Saudi Arabia for funding this research work through the project number “IFPHI: 352-155-2020”.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

The authors extend their appreciation to the Deputyship for Research & Innovation, Ministry of Education in Saudi Arabia for funding this research work through the project number “IFPHI-352-155-2020” and King Abdulaziz University, DSR, Jeddah, Saudi Arabia.

Conflicts of Interest

The authors declare no conflict of interest.

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Agriculture 12 01748 g001 550
Figure 1. The SEM image of shrimp waste biochar.
Figure 1. The SEM image of shrimp waste biochar.
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Agriculture 12 01748 g002 550
Figure 2. Effect of shrimp-waste-derived biochar (SWB) rates in photosynthetic pigments in quinoa leaves. C, SWB1, and SWB2 are 0, 1, and 2% (w/w) of biochar. (A) chlorophyll and (B) carotenoids. Means (±SD, n = 5) with different letters indicate significant differences.
Figure 2. Effect of shrimp-waste-derived biochar (SWB) rates in photosynthetic pigments in quinoa leaves. C, SWB1, and SWB2 are 0, 1, and 2% (w/w) of biochar. (A) chlorophyll and (B) carotenoids. Means (±SD, n = 5) with different letters indicate significant differences.
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Agriculture 12 01748 g003 550
Figure 3. Effect of shrimp-waste-derived biochar (SWB) rates in the growth of quinoa. C, SWB1, and SWB2 are 0, 1, and 2% (w/w) of biochar. (A) plant height, (B) fresh weight, and (C) dry weight. Means (±SD, n = 5) with different letters indicate significant differences.
Figure 3. Effect of shrimp-waste-derived biochar (SWB) rates in the growth of quinoa. C, SWB1, and SWB2 are 0, 1, and 2% (w/w) of biochar. (A) plant height, (B) fresh weight, and (C) dry weight. Means (±SD, n = 5) with different letters indicate significant differences.
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Agriculture 12 01748 g004 550
Figure 4. Effect of shrimp-waste-derived biochar (SWB) rates in metal concentrations in quinoa leaves. C, SWB1, and SWB2 are 0, 1, and 2% (w/w) of biochar. (A) Fe, (B) Mn, (C) Zn, (D) Cu, (E) Cd, and (F) Pb. Means (±SD, n = 5) with different letters indicate significant differences. Cd and Pb were below detection in the case of freshwater.
Figure 4. Effect of shrimp-waste-derived biochar (SWB) rates in metal concentrations in quinoa leaves. C, SWB1, and SWB2 are 0, 1, and 2% (w/w) of biochar. (A) Fe, (B) Mn, (C) Zn, (D) Cu, (E) Cd, and (F) Pb. Means (±SD, n = 5) with different letters indicate significant differences. Cd and Pb were below detection in the case of freshwater.
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Agriculture 12 01748 g005 550
Figure 5. Effect of shrimp-waste-derived biochar (SWB) rates in some biochemicals in quinoa leaves. C, SWB1, and SWB2 are 0, 1, and 2% (w/w) of biochar. (A) ascorbate peroxidase (APO), (B) polyphenol oxidase (PPO), (C) malondialdehyde (MDA), and (D) hydrogen peroxide (H2O2). Means (±SD, n = 5) with different letters indicate significant differences.
Figure 5. Effect of shrimp-waste-derived biochar (SWB) rates in some biochemicals in quinoa leaves. C, SWB1, and SWB2 are 0, 1, and 2% (w/w) of biochar. (A) ascorbate peroxidase (APO), (B) polyphenol oxidase (PPO), (C) malondialdehyde (MDA), and (D) hydrogen peroxide (H2O2). Means (±SD, n = 5) with different letters indicate significant differences.
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Figure 6. Schematic diagram shows the role of shrimp-waste-derived biochar (SWB) in improving the metal stress resistance of wastewater-irrigated quinoa.
Figure 6. Schematic diagram shows the role of shrimp-waste-derived biochar (SWB) in improving the metal stress resistance of wastewater-irrigated quinoa.
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Table
Table 1. Characterization of shrimp-waste-derived biochar (SWB). nd = not detected.
Table 1. Characterization of shrimp-waste-derived biochar (SWB). nd = not detected.
Organic-C
(g kg−1)		pHSalinity
(dS m−1)		N
(%)		P
(%)		K
(%)		Ca
(%)		Fe
(mg kg−1)		Mn
(mg kg−1)		Zn
(mg kg−1)		Cu
(mg kg−1)		Pb
(mg kg−1)		Cd
(mg kg−1)
420 ± 167.86 ± 0.084.12 ± 0.285.2 ± 0.14.1 ± 0.23.5 ± 0.125 ± 370 ± 435 ± 46.2 ± 0.23.5 ± 0.1ndnd
Table
Table 2. Basic soil characteristics.
Table 2. Basic soil characteristics.
Properties (Units)Value
TextureSandy
pH (1:2)7.80 ± 0.05
Organic Carbon (g kg−1)5.2 ± 0.2
Available N (mg kg−1)15 ± 1
Available P (Olsen) (mg kg−1)4.5 ± 0.1
Available K (mg kg−1)117 ± 10
Available Fe (mg kg−1)5.2 ± 0.3
Available Mn (mg kg−1)3.5 ± 0.2
Available Zn (mg kg−1)1.2 ± 0.1
Available Cu (mg kg−1)0.55 ± 0.08
Available Cd (mg kg−1)not detected
Available Pb (mg kg−1)not detected
Table
Table 3. Some chemical characteristics of fresh and wastewater.
Table 3. Some chemical characteristics of fresh and wastewater.
PropertiesFreshwaterWastewater* Permissible Limits
Organic carbon-15
Total soluble salts (dS m−1)0.55 ± 0.082.50 ± 0.12-
pH7.23 ± 0.046.71 ± 0.06-
Nitrogen (mg L−1)-3.5
Phosphorus (mg L−1)-6.5
Potassium (mg L−1)-22
Fe (mg L−1)0.05 ± 0.000.8 ± 0.15.0
Mn (mg L−1)0.04 ± 0.001.0 ± 0.20.2
Zn (mg L−1)0.07 ± 0.011.50 ± 0.322.0
Cu (mg L−1)0.03 ± 0.011.2 ± 0.030.2
Cd (mg L−1)nd0.08 ± 0.020.01
Pb (mg L−1)nd5.5 ± 0.25.0
* Permissible limits according to FAO (1985). nd = not detected.
Table
Table 4. Effect of shrimp-waste-derived biochar (SWB) rates on some soil characteristics and availability of heavy metals after harvesting quinoa plants. C, SWB1, and SWB2 are 0, 1, and 2% (w/w) of biochar. Means (±SD, n = 5) with different letters indicate significant differences. nd = not detected. The detection limits for Cd and Pb are: 0.07 and 1.06 µg L−1, respectively.
Table 4. Effect of shrimp-waste-derived biochar (SWB) rates on some soil characteristics and availability of heavy metals after harvesting quinoa plants. C, SWB1, and SWB2 are 0, 1, and 2% (w/w) of biochar. Means (±SD, n = 5) with different letters indicate significant differences. nd = not detected. The detection limits for Cd and Pb are: 0.07 and 1.06 µg L−1, respectively.
Water TypeTreatmentspHOrganic-C
(g kg−1)		Fe
(mg kg−1)		Zn
(mg kg−1)		Mn
(mg kg−1)		Cu
(mg kg−1)		Pb
(mg kg−1)		Cd
(mg kg−1)
FreshwaterC7.82 ± 0.04 b5.3 ± 0.1 c5.0 ± 0.2 b1.2 ± 0.1 c3.2 ± ±0.1 d0.53 ± 0.04 cndnd
SWB17.88 ± 0.03 ab5.8 ± 0.2 b4.9 ± 0.2 b1.2 ± 0.2 c3.3 ± 0.1 d0.52 ± 0.05 cndnd
SWB27.94 ± 0.02 a5.8 ± 0.1 b4.9 ± 0.3 b1.1 ± 0.1 c3.4 ± 0.1 d0.51 ± 0.09 cndnd
WastewaterC7.52 ± 0.06 c5.2 ± 0.2 c6.7 ± 0.2 a1.9 ± 0.2 a5.2 ± 0.2 a0.68 ± 0.05 a0.87 ± 0.14 a0.25 ± 0.03 a
SWB17.81 ± 0.02 b6.2 ± 0.1 a5.3 ± 0.1 b1.6 ± 0.2 ab4.8 ± 0.1 b0.62 ± 0.07 b0.63 ± 0.09 b0.21 ± 0.06 b
SWB27.83 ± 0.01 b6.4 ± 0.2 a5.2 ± 0.1 b1.4 ± 0.3 b4.2 ± 0.2 c0.60 ± 0.08 b0.57 ± 0.08 c0.18 ± 0.04 c
Table
Table 5. Effect of shrimp-waste-derived biochar (SWB) rates on nitrogen (N), phosphorous (P), potassium (K), and calcium (Ca) availability in soil. C, SWB1, and SWB2 are 0, 1, and 2% (w/w) of biochar. Means (±SD, n = 5) with different letters indicate significant differences.
Table 5. Effect of shrimp-waste-derived biochar (SWB) rates on nitrogen (N), phosphorous (P), potassium (K), and calcium (Ca) availability in soil. C, SWB1, and SWB2 are 0, 1, and 2% (w/w) of biochar. Means (±SD, n = 5) with different letters indicate significant differences.
Water TypeTreatmentsNPKCa
Available in Soil (mg kg−1)
FreshwaterC12 ± 1 c4.3 ± 0.2 c115 ± 8 d200 ± 12 f
SWB120 ± 1 b8.9 ± 0.3 b170 ± 7 c250 ± 11 d
SWB224 ± 1 a9.5 ± 0.2 b180 ± 5 b300 ± 16 b
WastewaterC15 ± 2 c5.2 ± 0.3 c118 ± 8 d210 ± 12 e
SWB125 ± 3 a9.1 ± 0.4 b184 ± 7 b270 ± 11 c
SWB228 ± 2 a11.6 ± 0.3 a195 ± 5 a320 ± 16 a
Table
Table 6. Effect of shrimp-waste-derived biochar (SWB) rates on nitrogen (N), phosphorous (P), potassium (K), and calcium (Ca) concentrations in plant shoot. C, SWB1, and SWB2 are 0, 1, and 2% (w/w) of biochar. Means (±SD, n = 5) with different letters indicate significant differences.
Table 6. Effect of shrimp-waste-derived biochar (SWB) rates on nitrogen (N), phosphorous (P), potassium (K), and calcium (Ca) concentrations in plant shoot. C, SWB1, and SWB2 are 0, 1, and 2% (w/w) of biochar. Means (±SD, n = 5) with different letters indicate significant differences.
Water TypeTreatmentsNPKCa
Shoot Concentrations (g kg−1)
FreshwaterC28 ± 2 c2.0 ± 0.1 c27 ± 1 c32 ± 3 c
SWB134 ± 3 b2.8 ± 0.1 b33 ± 2 b38 ± 5 b
SWB238 ± 2 ab3.4 ± 0.1 a37 ± 2 a42 ± 4 a
C30 ± 1 c2.2 ± 0.1 c29 ± 1 c33 ± 1 c
WastewaterSWB136 ± 3 b2.9 ± 0.1 b34 ± 2 b39 ± 3 b
SWB240 ± 3 a3.6 ± 0.1 a39 ± 2 a43 ± 3 a
Table
Table 7. Effect of shrimp-waste-derived biochar (SWB) rates in metal concentrations in quinoa seeds. C, SWB1, and SWB2 are 0, 1, and 2% (w/w) of biochar. Means (±SD, n = 5) with different letters indicate significant differences. Cd and Pb were below detection in the case of fresh water.
Table 7. Effect of shrimp-waste-derived biochar (SWB) rates in metal concentrations in quinoa seeds. C, SWB1, and SWB2 are 0, 1, and 2% (w/w) of biochar. Means (±SD, n = 5) with different letters indicate significant differences. Cd and Pb were below detection in the case of fresh water.
Water TypeTreatmentsFe
(mg kg−1)		Mn
(mg kg−1)		Zn
(mg kg−1)		Cu
(mg kg−1)		Pb
(mg kg−1)		Cd
(mg kg−1)
FreshwaterC169 ± 15 c87 ± 0.1 c67 ± 2 d53 ± 3 cndnd
SWB1168 ± 24 c86 ± 0.2 c70 ± 2 d52 ± 4 cndnd
SWB2170 ± 23 c88 ± 0.1 c71 ± 3 d51 ± 2 cndnd
WastewaterC220 ± 17 a97 ± 0.2 a90 ± 5 a70 ± 3 a0.52 ± 0.10 a0.38 ± 0.08 a
SWB1212 ± 18 b91 ± 0.2 b85 ± 4 b64 ± 4 b0.46 ± 0.10 b0.25 ± 0.07 b
SWB2210 ± 22 b90 ± 0.3 b79 ± 3 c62 ± 3 b0.19 ± 0.12 c0.14 ± 0.06 c
MPV42510099730.300.20
MPV: WHO/FAO [1] maximum permissible values (mg/kg) as per Eissa and Negim [5].
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Mousa, M.A.A.; Abo-Elyousr, K.A.M.; Ibrahim, O.H.M.; Alshareef, N.O.; Eissa, M.A. Shrimp-Waste-Derived Biochar Induces Metal Toxicity Tolerance of Wastewater-Irrigated Quinoa (Chenopodium quinoa). Agriculture 2022, 12, 1748. https://doi.org/10.3390/agriculture12111748

AMA Style

Mousa MAA, Abo-Elyousr KAM, Ibrahim OHM, Alshareef NO, Eissa MA. Shrimp-Waste-Derived Biochar Induces Metal Toxicity Tolerance of Wastewater-Irrigated Quinoa (Chenopodium quinoa). Agriculture. 2022; 12(11):1748. https://doi.org/10.3390/agriculture12111748

Chicago/Turabian Style

Mousa, Magdi A. A., Kamal A. M. Abo-Elyousr, Omer H. M. Ibrahim, Nouf Owdah Alshareef, and Mamdouh A. Eissa. 2022. "Shrimp-Waste-Derived Biochar Induces Metal Toxicity Tolerance of Wastewater-Irrigated Quinoa (Chenopodium quinoa)" Agriculture 12, no. 11: 1748. https://doi.org/10.3390/agriculture12111748

APA Style

Mousa, M. A. A., Abo-Elyousr, K. A. M., Ibrahim, O. H. M., Alshareef, N. O., & Eissa, M. A. (2022). Shrimp-Waste-Derived Biochar Induces Metal Toxicity Tolerance of Wastewater-Irrigated Quinoa (Chenopodium quinoa). Agriculture, 12(11), 1748. https://doi.org/10.3390/agriculture12111748

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