1. Introduction
The availability of freshwater used for irrigation in arid and semi-arid regions is declining rapidly [
1,
2,
3] and it is expected to be reduced even further due to global climate warming [
3,
4]. As a result, agricultural areas in arid and semi-arid areas often rely on wastewater and/or groundwater to satisfy their irrigation requirements [
2,
4,
5,
6]. This practice has many advantages and disadvantages, but if well managed (e.g., crops not consumed directly by humans) and properly monitored, it could contribute to food security and to the sustainability of water and soil resources [
6,
7].
The use of treated wastewater (TWW) for irrigation, besides providing much-needed water under arid and semi-arid conditions, practically eliminates the need for nitrogen fertilization, increases soil fertility, diminishes the risk of eutrophication, and saves energy [
2]. However, TWW also contains salts, heavy metal(loid)s (HMs), emerging contaminants, and pathogens that may degrade the soil and crops [
8,
9,
10,
11]. Groundwater (GW) used for irrigation is also required to meet quality guidelines [
12] with respect to e.g., salinity, as some Na salts are toxic to plants, in addition to toxic contaminants such as As, Se, and Cd, emergent contaminants, and pathogens. A particular concern is represented by staple foods contaminated with As due to the widespread contamination of As in groundwater worldwide [
13], its toxic nature [
14], and the relatively high mobility from soil to plant [
15]. Other toxic metals generally studied in conjunction with As include cadmium (Cd) and lead (Pb). Oddly, studies on the uptake of As by barley and oats are very few, among them [
16,
17,
18,
19], despite these being common staple cereals. Barley growing in soil containing about 11 mg kg
−1 of As had 0.10 mg kg
−1 of As in leaves and 0.65 mg kg
−1 of As in roots, while oats growing in the same soil had 0.27 mg kg
−1 of As in leaves and 0.73 mg kg
−1 of As in roots [
16]. Reports on As uptake by wheat are relatively few as well, and report a small uptake of As compared to the uptake of other metals [
4]. In contrast, there are multiple studies on the As content in rice growing in southeast Asia, since rice is a staple food and also a well-known As accumulator [
20,
21]. An information gap thus exists about the As uptake by crops other than rice that grow in semiarid areas such as the north of Mexico and the US Southwest, where the As sources, soil, and climatic conditions are quite different to those of Southeast Asia [
22].
The toxicity of HMs to plants varies according to multiple factors, including concentration, the presence of other toxicants, climatic conditions, and the plant’s own diverse physiological, biochemical, and molecular mechanisms against toxic substances [
19,
23,
24]. As a result, the negative impacts to crop and soil irrigated with GW or TWW are highly variable depending on the type of contaminants present and their concentrations, irrigation frequency, climate, and soil and aquifer type [
2,
4,
25]. Therefore, the response of crops and agricultural soil to the contaminants in irrigation water should be determined for each situation, often using field and greenhouse experiments [
8,
23,
26,
27].
Studies agree that bioaccumulation of metals and emergent contaminants in soils and crops may produce negative effects on human and ecosystem health, especially after long-term wastewater irrigation [
1,
9,
28]. The expected health risks to humans are a function of the metal and the amount of metal bioaccumulation in crops. For example, Cao et al. [
29] tested twenty crops and six HMs using pot experiments and identified three crops and three toxicants that posed a higher health risk to the population.
Crops used for fodder, such as barley and oats, are a favored choice of crop growing in soil rich in HMs because they are not directly consumed by humans and their resistance to the presence of heavy metals [
19,
30]. In addition to their tolerance to toxic metals [
19], these crops, as well as other cereals, respond favorably to wastewater irrigation compared to well water with an increase in seed yield and leaf chlorophyll [
8,
27].
Regulations and recommended guidelines for the safe use of wastewater in agriculture are reported by various agencies, including the FAO, WHO, and US EPA, in addition to those issued by individual countries. However, most of these lists generally include only a few HMs. Seventy such guidelines for agricultural purposes from around the world were compiled into a review by Shoushtarian and Negahban-Azar [
25]. Notably, a set of recommended values for HMs in TWW used for irrigation in arid and semiarid areas of Texas vary according to short- or long-term irrigation [
31]. The values reported for short-term (<20 years) irrigation coincide with the values reported by the FAO [
32]. Recommended guidelines for HMs in cereal grains are 0.2 mg kg
−1 of As, 0.1 mg kg
−1 of Cd, and 0.02 mg kg
-1 of Pb [
12].
The objectives of this study were to: identify the extent to which As, Cd, and Pb incorporate into barley (Hordeum vulgare L.) and oats (Avena sativa L.) after irrigating with TWW or GW; determine the bioaccumulation and translocation of HMs for each crop; to make recommendations based on the potential accumulation of As, Cd, and Pb over long-term irrigation in this water-scarce region whose groundwater contains geogenic As.
4. Discussion
The soil of the studied area has been irrigated with TWW for several decades, a period long enough to allow the soil to stabilize with respect to solutes contained in TWW, including HMs, nutrients, and organic matter (
Table 3 and
Table 4) and resulting in a soil containing 19 mg kg
−1 of As. This is the first report of As content in soils in this region and fits within the reported 33.0 mg kg
−1 of As in sediments of the nearest reservoir, 20.3 mg kg
−1 of As in river sediment, and 10.2 mg kg
−1 of As background value [
34]. Irrigation water, either as TWW or GW, contained about the same concentration of As, about 0.045 mg L
−1 of As, which surpassed the recommended guidelines of both Mexico (0.025 mg L
−1) and the WHO (10 mg L
−1). The uptake of As into barley and oats has not been previously reported for northern Mexico, despite this area ranking first in Mexico’s oat production.
In plants, As accumulated primarily in the roots and least in grain in either barley or oats, as shown in
Table 5 and
Table 6. The As content in each part of the plant (root, leaves, stem, and grain) was the same (according to Levene’s test) between plants irrigated with GW and those irrigated with TWW. However, there was a significant difference (p < 0.05) in the As content between barley and oats for each of the grains, stems, and roots.
Although botanically similar, HMs accumulation in grains of barley or oats differed significantly; oats accumulated more As than barley despite the fact that the As in roots was about the same in either crop, in agreement with other studies [
16]. The edible part of both plants is the grain, however, the leaves and stems may also be used as fodder for cattle. The grain of barley contained As values at or near the recommended guidelines (0.2 mg kg
−1) whereas leaves contained about 1.5 mg kg
−1 of As. In oats, the amount of As in grains was about twice the amount in barley but the leaves accumulated slightly less As. The As content in barley grains fell within values reported for other world regions, 0.04 – 0.07 mg kg
−1 [
16,
44].
The difference in metal uptake and translocation between barley and oats has been explained by their different mechanisms to deal with metal stress, either producing an increase (oats) or decrease (barley) in soluble sugars and protein in plant tissue [
17,
19,
45]. The amount of metal assimilated by plants is reported to be a function of many factors, including temperature, soil mineralogical and bacteriological composition, HMs, and organic matter content [
24]. For As, its speciation as either arsenite or arsenate has also been reported to affect accumulation, with arsenite uptake being several times greater than arsenate uptake (Su et al. 2010) [
20]. The alkaline conditions of both soil and water in this study suggest that As occurs primarily as arsenate. The similar soil chemistry and temperature of the various samples collected within the study area (
Table 3) indicate a relatively homogeneous soil. Therefore, the differences in metal accumulation are due to the inherent uptake and translocation mechanisms of either barley or oats and the solutes present in the irrigation water. Also, differences between GW and TWW were not statistically significant with respect to their content of TDS, As, and other solutes, except for phosphate, which was enriched in TWW (
Table 1) and is relevant to this study as it aids in the accumulation and translocation of As [
24]. However, the difference in phosphate was not large enough to have an effect on the accumulation of As in either barley or oats (
Table 5 and
Table 6).
A measure of the bioaccumulation and translocation of metals in plants is compiled in
Table 6. The bioaccumulation factor BCF < 1 obtained for As in barley indicates that this plant is tolerant to As and it is not an accumulator, as has been reported for other regions in Mexico [
18,
19] and elsewhere [
16,
20,
44,
45]. The results obtained here for barley growing in a soil containing 19 mg kg
−1 of As also agree with the tolerance reported by a study using soil spiked with several concentrations of As [
45], where the BCF and TF of barley growing in soils up to 50 mg kg
−1 remained unchanged and an accumulation was first observed when the As content in soil was about 100 mg kg
−1.
BCF, TF
grain, and TF
leaves were all < 1 for As, Cd, and Pb in both crops, except for Pb in the root and leaves of oats, where values up to 2.17 for BCF were obtained (
Table 6). However, leaves contain three-fold the amount of Pb compared to stems, for which combining leaves and stems for cattle feed would result in a smaller Pb content compared to that of leaves alone.
The tolerance of barley and oats to As has been documented by several studies [
19,
27,
44], often comparing it to rice. The As uptake and translocation are reportedly facilitated by phosphate and silicon transporters [
14,
24], as well as by organic matter (OM). HMs translocate from the root to shoots through xylem vessels and are deposited in vacuoles where they remain removed from cytosol [
23]. The increase in soil OM content may result in the reducing of conditions that favor the reduced form of As, arsenite, to be uptaken, as well as conditions that increase the mobility of As in soil and the bioavailability of As to plants [
24]. However, these mechanisms are particular to As and do not necessarily apply to Cd and Pb. Cd accumulation is facilitated by Mn, Fe, and Zn transporters, whereas the mechanisms responsible for the uptake and translocation of Pb are not completely known [
14,
17].
Phytoremediation is one of the most recommended treatments to reduce metal content in soils. This is achieved using hyperaccumulator plants, several of which have been identified for each metal [
23]. Growing crops that are tolerant to metals is a variation of this strategy [
29] since plants can be altered genetically to diminish their metal uptake [
14]. A suite of soil amendments can also increase the tolerance of plants to HMs and reduce the uptake, among them are thiol-rich compounds [
14,
24].
Barley and oats are tolerant to salinity and grow well in semiarid areas. Our results found a low As content in grains and a moderate As content in the leaves of both. Therefore, these crops offer a viable alternative to growing foodstuff while removing nutrients from TWW. The accumulation of As in soil was low to moderate (19 mg kg
−1) after decades of being irrigated with TWW and the As content in grain was low (0.02 to 0.04 mg kg
−1) at a level listed as safe by FAO [
12]. Other metal content attenuation factors in plants and soil, respectively, are the non-linear increase in metals in crops with respect to metals in soil [
1,
4,
46] and the periodic flushing of contaminants during the intense rain showers that typically occur in this region every five years or so [
35]. Nevertheless, conscientious monitoring of HMs in soil and plants is recommended.
5. Conclusions
The results reported here fill an important gap in the knowledge on the uptake of As by two little-studied cereal crops, barley and oats, grown under alkaline soils in semiarid areas. The As uptake of barley and oats was low for the grain and moderate for leaves, suggesting that cultivation of these forage crops contributes to the sustainable management of water resources by removing nutrients from TWW and reducing the amount of GW extracted for irrigation. These processes contribute considerably to the conservation of water in this water-scarce area.
No significant difference in As content was found between TWW and GW nor between crops irrigated with TWW or GWW, despite TWW containing more phosphate (a known As transporter) than GW but there was a significant difference between barley and oats, with an increased As content in oats. Bioaccumulation and translocation factors were <1 for As in both crops, indicating that these plants are not accumulators of As. A spinoff result of this study was the finding that oat leaves accumulated lead, albeit slightly (BCF 1.4, TFleaf 1.4). However, the TF for oat grains remained below 1.
Based on the above results, the cultivation of barley and/or oats is recommended as a safe and sustainable practice in this agricultural region whose groundwater contains high concentrations of geogenic As. Although neither barley nor oat accumulated As or Cd in any parts of the plant, barley plants outperformed oats based on their lesser uptake of As, Cd, and Pb. Close monitoring of the content of As and heavy metals in plants and soil is recommended. Studies determining other toxic solutes potentially present, such as emergent contaminants, are needed.