Evaluation of the Impacts of Salinity on Biomass and Nutrient Levels of Agave Species with Agricultural Potential in Semiarid Regions

in HortScience

Long used as a source of food, beverages, and fiber, Agave exhibits potential to be cultivated as a crop to produce alternative sweeteners, bioenergy, and a variety of other end uses. However, little is known regarding the productivity levels of Agave when grown in saline soils in semiarid regions. Hydroponic experiments were carried out to evaluate the effects of salinity on biomass accumulation and nutrient levels of young plants of Agave parryi, Agave utahensis ssp. kaibabensis, Agave utahensis ssp. utahensis, and Agave weberi. Salinity treatments (0.6, 3.0, 6.0, and 9.0 dS·m−1) were imposed in each experiment. Both subspecies of A. utahensis were sensitive to salt treatments. In the higher salinity treatments, A. utahensis ssp. utahensis exhibited high mortality; both subspecies had lower plant dry weights. Agave parryi was more tolerant, but experienced a decrease in plant dry weight in the 9.0 dS·m−1 treatment. The biomass of A. weberi was unaffected by any level of salinity. Calcium, Mg, S, and Mn levels decreased in both A. parryi and A. weberi at higher salinity levels. Potassium and P levels in A. parryi decreased in the higher salt treatments. Decreases in nutrients were not severe enough to cause any apparent nutrient deficiencies in A. parryi and A. weberi. Agave parryi and A. weberi tolerated salinity at higher levels than expected, and may show promise for cultivation in saline soils.

Abstract

Long used as a source of food, beverages, and fiber, Agave exhibits potential to be cultivated as a crop to produce alternative sweeteners, bioenergy, and a variety of other end uses. However, little is known regarding the productivity levels of Agave when grown in saline soils in semiarid regions. Hydroponic experiments were carried out to evaluate the effects of salinity on biomass accumulation and nutrient levels of young plants of Agave parryi, Agave utahensis ssp. kaibabensis, Agave utahensis ssp. utahensis, and Agave weberi. Salinity treatments (0.6, 3.0, 6.0, and 9.0 dS·m−1) were imposed in each experiment. Both subspecies of A. utahensis were sensitive to salt treatments. In the higher salinity treatments, A. utahensis ssp. utahensis exhibited high mortality; both subspecies had lower plant dry weights. Agave parryi was more tolerant, but experienced a decrease in plant dry weight in the 9.0 dS·m−1 treatment. The biomass of A. weberi was unaffected by any level of salinity. Calcium, Mg, S, and Mn levels decreased in both A. parryi and A. weberi at higher salinity levels. Potassium and P levels in A. parryi decreased in the higher salt treatments. Decreases in nutrients were not severe enough to cause any apparent nutrient deficiencies in A. parryi and A. weberi. Agave parryi and A. weberi tolerated salinity at higher levels than expected, and may show promise for cultivation in saline soils.

Throughout the world, groundwater levels have been in continual decline (Konikow, 2013; Wada et al., 2010), which could potentially lead to local and regional water shortages, especially in areas that require large water inputs to sustain crop production (Dominguez-Faus et al., 2009). Such limitations increase the need for identifying plant species that generate high yields despite constraints on water availability. Indeed, exploiting the crop potential of select Agave spp. could help reconcile disparities related to growing populations and dwindling water reserves in semiarid regions, such as the southwestern United States. Agaves employ the crassulacean acid metabolism (CAM) photosynthetic pathway, which maximizes water-use efficiency by shifting most CO2 uptake to the night (Borland et al., 2009; Nobel, 2010; Yang et al., 2015). Cooler nighttime temperatures reduce the vapor pressure gradient between their leaves and the air, resulting in markedly lower transpiration rates as compared with C3 and C4 plants (Griffiths, 1988; Winter and Smith, 1996). Consequently, CAM confers the ability to agaves to be highly water-use efficient in hot, drought-prone environments.

Most agaves, however, lack sufficient cold hardiness to survive winters in high-elevation deserts (Nobel, 1996), but some species appear to be sufficiently cold hardy. Agave parryi, A. utahensis, and A. weberi can tolerate temperatures as low as −19.6, −17.5, and −9.8 °C, respectively (Nobel, 1984; Nobel and Smith, 1983; Parida and Das, 2005), suggesting they have potential to be grown in more northern regions of the southwestern United States at elevations up to 850 m. Agave parryi is native to the southwest, and is found in mountainous areas of central and northern Arizona, southwestern New Mexico, and northern Chihuahua (Minnis and Plog, 1976). Agave utahensis populates mountain slopes of southern Utah, southern Nevada, northwestern Arizona, and southeastern California (Baldwin et al., 2012; Welsh et al., 1993). The native distribution of A. weberi ranges from southern Texas to San Luis Potosi and Tamaulipas, Mexico (eMonocot Team, 2012).

Traditionally, agaves were used for food, beverage, and fiber (Castetter et al., 1938). Nowadays, however, Agave shows promise as a bioenergy crop (Conlu et al., 2011; Davis et al., 2011; Escamilla-Trevino, 2012; Holtum et al., 2011; Nunez et al., 2011), which is underscored by the high productivity of Agave mapisaga and Agave salmiana. Both were reported by Nobel (1991) to have yielded 38 and 42 Mg·ha−1·year−1, respectively, which exceeds that of other feedstock crops, such as corn (Zea mays) (15–19 Mg·ha−1·year−1) (Dohleman and Long, 2009) and switchgrass (Panicum virgatum) (10–12 Mg·ha−1·year−1) (Heaton et al., 2008). In addition, the high biomass and putative cold hardiness of mature A. weberi (Gentry, 1982; Irish and Irish, 2000) plants suggest that this species could be produced as a bioenergy crop.

However, salinity could severely impede cultivation of A. parryi, A. utahensis, and A. weberi in many semiarid regions. In the United States, 8.5 million ha of land are considered saline or sodic (Massoud, 1976). Over half of this land area is located in the western United States (Bohn et al., 1985). Excess salinity can decrease water availability to plants because the osmotic pressure of the soil solution increases as the salt concentration increases, resulting in stunted plant growth (Abrol et al., 1988). In addition, high salt concentrations can reduce cell expansion in root tips and young leaves, leading to stomatal closure and reduced water uptake (Munns and Tester, 2008). Excessive salt absorption can cause plants to suffer ionic stress due to ion accumulation in shoots (Munns and Tester, 2008), leading other nutrient ions such as Ca2+, K+, and Mg2+ to become deficient because they have to compete with high NaCl uptake (Khan et al., 1999).

The impact of high salinity on yield of many C3 and C4 crops is well documented. Corn yield decreased by 23% at an electrical conductivity (EC) level of 3.4 dS·m−1 (Katerji et al., 1996). Similarly, soybean (Glycine max) had a 56% decrease in yield at 6.7 dS·m−1 (Katerji et al., 1998). Contrary to what is widely assumed, several succulent plant species do not exhibit a higher degree of resistance to salt stress than C3 and C4 plant species (Nobel and Berry, 1985). Cladodes of Opuntia ficus-indica decreased 40% in growth at 4.2 dS·m−1 NaCl (Nerd et al., 1991). Pineapple (Ananas comosus) can grow in soil with an EC range from 3.0 to 6.0 dS·m−1 before declining in growth (Ayers and Westcot, 1985). Aloe vera started to experience a decrease in leaf number and root dry weight at EC levels higher than 6.0 dS·m−1 (Moghbeli et al., 2012).

The tolerance of Agave to salinity varies depending on species. Nobel and Berry (1985) found that EC levels above 3.0 dS·m−1 greatly decreased elongation of roots and shoots of Agave deserti seedlings. Schuch and Kelly (2008) found that A. parryi shoot and root dry weights decreased at an EC of 5.0 dS·m−1. In addition, 10-month-old A. sisalana plants exposed to 10 dS·m−1 NaCl and 10 dS·m−1 CaCl2 had a reduction in dry weight of 40% after 5 months (El-Gamassy et al., 1974). In another study, the dry weight of A. sisalana decreased in EC levels of 6.3 dS·m−1, and decreased by 46% in EC levels of 25 dS·m−1 (El-Bagoury et al., 1993). However, in contrast to these findings, Miyamoto (2008) found that salinity did not have any impacts on Agave americana growth at levels up to 9.0 dS·m−1.

To gain a better understanding of how agaves respond to high salinity, more species need to be evaluated, particularly those of agricultural interest. The main objective of this study was to determine the impact of treatments ranging from low to high salinity had on productivity of young plants of A. weberi, A. parryi, and two subspecies of A. utahensis. If salinity severely impacts growth, cultivating or reestablishing these species for commercial purposes may not be feasible in dryland regions. This may particularly be the case in degraded, marginal lands where salinity exceeds normal thresholds. However, the tolerance of Agave to salinity appears to vary depending on species, suggesting that some species may be more tolerant to salinity than generally assumed. We hypothesized that A. parryi, A. utahensis, and A. weberi would be able to tolerate salinity levels up to 6.0 dS·m−1 before decreasing in productivity. On the basis of past research, 6.0 dS·m−1 appears to be the threshold at which growth and development of many Agave spp. begin to be impaired (El-Bagoury et al., 1993; Schuch and Kelly, 2008).

Materials and Methods

Experimental design, plant material, and location

Four separate species-level experiments were established to analyze the following Agave taxa: A. parryi, A. utahensis ssp. kaibabensis, A. utahensis ssp. utahensis, and A. weberi. The two subspecies of A. utahensis were evaluated in this study to gain a more comprehensive understanding of how the species responds overall to salinity. Because of limited plant availability, A. parryi and A. weberi plants used in the study were 24-week-old plants propagated through tissue culture (Rancho Tissue Technologies, Rancho Santa Fe, CA). Three-week-old A. utahensis ssp. kaibabensis and A. utahensis ssp. utahensis plants were grown from seed obtained from Phoenix Desert Nurseries (Phoenix, AZ). The study was conducted under greenhouse conditions at Brigham Young University in Provo, UT. Plants were grown under supplemental light (12 h daily) with average temperatures of 25 ± 5 °C during the light period and 15 ± 2 °C during the dark period. Relative humidity during the study period ranged from 6% to 75%, with a median value of 47%. Average photosynthetically active radiation was 287 μmol·m−2·s−1. All plants were grown in hydroponics. Hydroponic culture of seedlings has been found to be effective for screening for salinity tolerance in agaves (Nobel and Berry, 1985), other species (Munns and James, 2003; Shaheen and Hood-Nowotny, 2005), and for other forms of environmental stress tolerance (Bouslama and Schapaugh, 1984). In addition, young plants were selected instead of mature plants for the experiments to assess the impacts of salinity at the most susceptible stage of plant growth and development. When grown as crops, most agaves are planted as young seedlings, bulbils, or small vegetative offsets (Davis et al., 2011; Holtum et al., 2011; Nobel, 1994).

Each experiment was arranged in a randomized complete block design. The first (A. utahensis ssp. kaibabensis) and second (A. weberi) experiments began on 15 Nov. 2012, and concluded after 75 d. The third (A. parryi) and fourth (A. utahensis ssp. utahensis) experiments began on 20 Feb. 2013 and ended after 60 d. A container (diameter = 23 cm, height = 23.5 cm, volume = 9643 cm3) containing four plants was defined as the experimental unit. Four salinity treatments (0.6, 3.0, 6.0, and 9.0 dS·m−1) were established, with each treatment being replicated four times, resulting in a total of 16 containers in each experiment. The 0.6 dS·m−1 treatment served as the control. Containers were randomly placed in four rows ≈30 cm apart on a greenhouse bench.

Agave parryi.

Sixty-four plants were thoroughly washed to remove soil particles from roots. Plants were then transferred to 16 aluminum foil–covered polyethylene containers (depth = 24 cm, width = 24 cm, volume = 7.6 L), containing 7.5 L dilute, modified Steinberg nutrient solution (Nichols et al., 2012; Steinberg, 1953). The containers were randomly arranged on a greenhouse bench. Each plant was inserted into neoprene net cup lids and placed inside 5.1-cm foam-net pots (Atlantis Hydroponics, College Park, GA). Each foam-net pot was placed inside an opaque plastic lid situated on top of each container. Air stones (AIR-1000, Top Fin, Phoenix, AZ) were placed at the base of each container to aerate the roots and solution. Plants were grown in the pretreatment solution for 14 d before transfer into treatments.

The initial nutrient concentrations used during the treatment period were the same as the pretreatment, except NaCl (Sigma-Aldrich, St. Louis, MO) concentration was adjusted to reach the desired EC level for each treatment at the same time. EC was measured using a HM Digital COM-100 EC meter (Atlantis Hydroponics). Salinity was supplied at four levels (0.6, 3, 6, and 9.0 dS·m−1) of NaCl in nutrient solutions buffered at a pH of 6. Solution pH was initially adjusted and then maintained daily with sodium hydroxide and hydrochloric acid. Nutrient solutions in each container were replenished every 2 weeks. When replenishing the solutions, the whole container was replaced with a new solution in deionized water to ensure that salinity level would remain relatively constant over the course of the experiments. Seedlings were harvested after 60 d in treatment. Shoots and roots were separated for further analysis.

Agave utahensis ssp. kaibabensis.

Seeds were germinated by placing them on cheesecloth placed on 4-mm stainless steel screens in 9.5-cm deep rectangular plastic trays. The screens were immersed with 2 L of diluted modified Steinberg solution. Germination and subsequent elongation of seedlings occurred over a 21-d period at ≈25 °C. The pretreatment procedure applied to A. parryi was also used for A. utahensis ssp. kaibabensis. However, during the treatment period, nutrient solutions were replenished every 4 weeks instead of every 2 weeks. Seedlings were harvested after 75 d in treatment.

Agave utahensis ssp. utahensis.

Seedlings of A. utahensis ssp. utahensis were propagated similarly to those of A. utahensis ssp. kaibabensis. They were also pretreated and treated with the same modified Steinberg solutions as the A. parryi plants, except that 128 seedlings comparable in size were transferred to opaque plastic lids placed on top of containers (eight plants per container). After a 14-d pretreatment period, 64 seedlings uniform in size were then selected out of the 128 seedlings and transferred to new containers (four plants per container) with opaque plastic lids. The treatment protocol for A. parryi was used for A. utahensis ssp. utahensis except nutrient solutions were initially replenished every 2 weeks for the first 30 d. They were then replenished every 4 weeks due to slow growth rates. Seedlings were harvested after 60 d in treatment.

Agave weberi.

Plants of A. weberi were pretreated and treated with the same modified Steinberg solution as the A. parryi plants. However, during the treatment period, nutrient solutions were replenished 4 weeks after treatment started. Following the initial replenishment, nutrient solutions were replenished every 2 weeks. Seedlings were harvested after 60 d in treatment.

Mortality count, dry weight, and elemental analysis

At the end of each experiment, a mortality count was taken to determine the percent mortality of plants in each treatment. Shoots and roots of plants in all experiments were oven dried at 65 °C for a minimum of 72 h to uniform dryness and then weighed. Shoots of A. parryi and A. weberi were subsequently ground using a mortar and pestle for elemental analysis. Shoots of A. utahensis ssp. kaibabensis and A. utahensis ssp. utahensis were not ground because there was not enough dry material to use for elemental analysis. To measure the concentrations of Ca, Mg, K, P, S, Zn, Cu, and Na in the shoots, 0.5 g of each sample was digested for 12 h in 5 mL nitric-perchloric acid and analyzed by inductively coupled plasma atomic emission spectroscopy (IRIS Intrepid II XSP; Thermo Electron Corporation, Franklin, MD). In addition, 0.1 g of each sample was weighed in a tin capsule. The capsule was then combusted in a CHN analyzer (LECO CHN628 series; LECO Corporation, St. Joseph, MI) to estimate total C and N.

Statistical analysis

The average dry shoot, dry root, and nutrient concentrations were calculated from the four plants in each bucket for each of the species-level experiments. Statistical analyses were performed using Statistical Analysis System (SAS, version 9.3; SAS Institute, Cary, NC). Data for shoot dry weight, root dry weight, total dry weight, and nutrient uptake were analyzed using analysis of variance with mean separation using the Tukey–Kramer test at the 0.05 level of significance (P ≤ 0.05). A control for normality for each analysis was accomplished with quantile–quantile plots for residuals, and by running the Shapiro–Wilk, Cramer–von Mises, and Anderson–Darling tests.

Because of the binary nature of the data, plant survival was analyzed with analysis of deviance using the glm() function in R [version 3.0.2 (R Development Core Team, 2013)]. A binomial distribution was specified for each generalized linear model (i.e., one for each subspecies). A series of Tukey contrasts using the multcomp package (Hothorn et al., 2008) were run to assess differences in survival among the treatments. The 0.6 dS·m−1 (control) treatment was removed before this analysis as no mortality was noted within this treatment. This situation (i.e., all success or failure) is problematic with binomial data as standard errors are inflated to a point where statistical differences cannot be discerned.

Results

Mortality.

Across salinity treatments, there were no differences in mortality of seedlings of A. utahensis ssp. kaibabensis (P = 0.36) (Table 1). As EC levels increased, there was a corresponding increase in mortality of A. utahensis ssp. utahensis seedlings. Mortality in the 9.0 dS·m−1 treatment was ≈25%, 50%, and 75% higher than in the 6.0, 3.0, and 0.6 dS·m−1 treatments. The mortality of plants in the 9.0 dS·m−1 treatment exceeded those in the 3.0 dS·m−1 treatment. All A. parryi and A. weberi plants survived, regardless of treatment (data not shown).

Table 1.

Percent mortality of 3-week-old seedlings of Agave utahensis ssp. kaibabensis and Agave utahensis ssp. utahensis exposed to four levels of salinity in hydroponic culture under greenhouse conditions for 75 and 60 d, respectively. Standard errors follow mortality mean values.

Table 1.

Shoot, root, and total dry weight.

Shoot, root, and total dry weights of A. parryi differed between plants in the control and 9.0 dS·m−1 treatments. Plants in the control treatment had the highest dry weight values (Table 2).

Table 2.

Four separate experiments evaluating the effects 0.6–9.0 dS·m−1 salinity levels had on shoot, root, and total dry weight of plants of four Agave spp. in hydroponic culture under greenhouse conditions. Twenty-four-week old plants of Agave parryi and 3-week-old seedlings of Agave utahensis ssp. utahensis were in treatment for 60 d, whereas 24-week-old plants of Agave weberi and 3-week-old plants of Agave utahensis ssp. kaibabensis were in treatment for 75 d. Standard errors follow mean values.

Table 2.

Seedlings of A. utahensis ssp. kaibabensis in the 6.0 and 9.0 dS·m−1 treatments had 1.5 to 2 times less shoot dry weight than those in the control treatment (Table 2). Roots in the 9.0 dS·m−1 treatment had nearly 2.5 times less dry weight than of those in the control treatment (Table 2). Total dry weight of plants in the control treatment exceeded that found in the 6.0 and 9.0 dS·m−1 treatments. Also, total dry weight of plants in the 3.0 dS·m−1 treatment was higher than of those in the 9.0 dS·m−1 treatment (Table 2).

Agave utahensis ssp. utahensis seedlings in the control treatment had more than two times as much shoot dry weight than those in the 9.0 dS·m−1 treatment (Table 2). Shoot dry weight of control seedlings also were 1.8 times greater than seedlings in the 6.0 dS·m−1 treatment (Table 2). Seedlings in the control treatment had 2.6 and 4.5 times more root dry weight, respectively, than seedlings in the 6.0 and 9.0 dS·m−1 treatments (Table 2). Treatment differences in total dry weight followed that of shoot and root dry weights. There were no differences in shoot, root, or total dry weights of A. weberi among the four treatments (Table 2).

Nutrient concentrations.

Carbon concentration of A. parryi in the 3.0 dS·m−1 treatment exceeded that in the 9.0 dS·m−1 treatment. Nitrogen concentration differed between the 3.0 and 6.0 dS·m−1 treatments, with more N in the 6.0 dS·m−1 treatment. There were no differences between the 0.6, 6.0, and 9.0 dS·m−1 treatments. Dried shoot samples indicated differences in Ca, K, Mg, Mn, Na, P, and S (Table 3). Calcium, K, Mg, Mn, and S concentrations all decreased with an increase in salt treatment. Each of these elements had decreases in the 6.0 and 9.0 dS·m−1 treatments relative to the control. Sodium levels increased correspondingly as the salt treatment increased. Phosphorus concentration was lower in the 9.0 dS·m−1 treatment relative to the 3.0 and 6.0 dS·m−1 treatments. There was also no difference in P concentration between the 0.6 and 9.0 dS·m−1 treatments (Table 3). However, zinc concentration in the control treatment exceeded that of all other treatments.

Table 3.

Nutrient concentrations of two separate species-level experiments evaluating the effects of salinity on nutrient uptake of 24-week-old plants of Agave weberi and Agave parryi in hydroponic culture under greenhouse conditions. Standard errors follow mean values.

Table 3.

There were no differences in C concentration between any of the treatments for A. weberi. Nitrogen concentration in plants in the control treatment was lower than of those in the other treatments (Table 3). There were no differences in K, P, Zn, and Fe among plants in the four treatments. However, Ca, Mg, S, and Mn all decreased in concentration as salinity increased, particularly in the 6.0 and 9.0 dS·m−1 treatments. Copper concentrations were lower in plants in the control and 9.0 dS·m−1 treatments compared with the 3.0 dS·m−1 treatment. Sodium concentration increased as salinity treatment increased (Table 3).

Discussion

Growth of both subspecies of A. utahensis was reduced at high salt concentrations. The poor response of these plants to salinity may have been due to their exposure to high levels of salt stress as seedlings. Their ability to adapt to salt stress was low compared with the more established and putatively stress-tolerant A. parryi and A. weberi plants. Nobel and Berry (1985) reported that 12-d-old seedlings of A. deserti also performed poorly in high salinity, with a 50% decrease in root growth occurring at 5.6 dS·m−1, and a similar decrease in shoot growth occurring at 9.3 dS·m−1.

To date, research has not been carried out determining how mature plants of A. utahensis ssp. kaibabensis and A. utahensis ssp. utahensis respond to high salinity. However, using soil-based data collected by Nobel and Berry (1985), Hara (1992) estimated that EC values of soils, where A. utahensis plants naturally establish, range between 2.5 and 3.2 dS·m−1. This possibly explains why the species is fairly intolerant of high salt concentrations. Another reason that A. utahensis ssp. kaibabensis and A. utahensis ssp. utahensis seedlings performed poorly may have been due to the inability of the plants to osmotically adjust to high salt levels. Mature Agave plants typically tolerate high salt concentrations through osmotic adjustment, where moisture content decreases and Na+ and Cl ions increase in the shoots (Peña-Valdivia and Sánchez-Urdaneta, 2009; Schuch and Kelly, 2008). Agave plants will also exclude salt from their leaves to adjust to salt stress. However, since the plants of both taxa in our study were only seedlings, their capacity to store salt was possibly limited. Although not directly measured, such adjustment mechanisms may have been at play with the larger A. parryi and A. weberi plants.

Data from the study suggest that A. parryi performs well in EC levels up to 6.0 dS·m−1, which is in line with another study that analyzed the salinity tolerance of 1-year-old A. parryi plants grown under greenhouse conditions (Miyamoto, 2008). Miyamoto (2008) found that plant growth was not restricted within the range of 6–8 dS·m−1, but was severely reduced at 9.4 dS·m−1. Contrary to our findings, Schuch and Kelly (2008) found that relative to field-grown A. parryi plants exposed to low-salinity conditions (0.6 dS·m−1), shoot and root dry weights of potted conspecific plants decreased by 33% when irrigated with water with an EC of 5 dS·m−1. This suggests that even within species, some conspecific Agave plants may be more tolerant to salinity than others.

Agave weberi was notably tolerant to high salinity levels, with no difference in growth among treatments. Other species of agaves have also done well in high salinity. Miyamoto (2008) found that A. americana plants were considerably tolerant of high salt levels, and did not have any decreases in growth when irrigated with 9.4 dS·m−1 water. In addition, soil samples taken from the root zones of field-grown A. americana had EC levels ranging between 7.0 and 8.0 dS·m−1 (Hara, 1992; Nobel and Berry, 1985). Interestingly, EC levels of soils were found to be exceedingly high where mature A. salmiana (13–16.0 dS·m−1), Agave lechuguilla (17–20 dS·m−1), and Agave foucroydes (44–47 dS·m−1) plants were growing (Hara 1992; Nobel and Berry, 1985). Successful establishment at such high salinity levels suggests that at least some Agave spp. exhibit appreciable salt tolerance.

To our knowledge, studies evaluating optimal nutrient concentrations of A. parryi and A. weberi have not been carried out. Moreover, identifying nutrient deficiencies in Agave spp. can be difficult because visual symptoms are not always obvious (Ruiz-Luna et al., 2011). Indeed, Ruiz-Luna et al. (2011) observed that nutritional deficiencies in agaves may not be manifest for up to 12 months. As such, it was difficult to visually determine if plants in our study were suffering from nutrient deficiencies. However, by taking into consideration reported nutrient concentrations of ecologically similar Agave spp. (A. americana, A. deserti, A. fourcroydes, A. lechuguilla, A. salmiana, and A. utahensis) (Nobel and Berry, 1985), estimates can be made of nutrient threshold levels of both A. parryi and A. weberi. For A. parryi and A. weberi, N uptake differed between treatments, but did not appear to be associated with salinity level. Agave weberi had less N in the control group than the 6.0 and 9.0 dS·m−1 treatments, whereas A. parryi had less N in the 3.0 dS·m−1 treatment than the 6.0 dS·m−1 treatment. The decrease in N in the lower treatments does not correlate with that found in other studies, where N tended to decrease with an increase in salinity (Al-Rawahy et al., 1992; Feigin et al., 1991; Pessarakli, 1991). However, salinity level does not necessarily affect overall N uptake (Maksimovic and Ilin, 2012). Salt-stressed plants may continue to accumulate N, even if the plants experience a reduction in yield or dry matter.

The decrease in N, however, did not appear to impair plant growth and productivity. Plant dry weight in the control and 3.0 dS·m−1 treatments exceeded that in the 6.0 and 9.0 dS·m−1 treatments. Compared with the average N content of six Agave spp. (1.19%) evaluated by Nobel and Berry (1985), the lowest N levels in A. parryi (1.97%) and A. weberi (3.28%) in our study were relatively high. This suggests that the plants in these treatments were likely not impaired by N deficiency.

In terms of the other essential nutrients that decreased, Ca appears to have been the only element that became deficient at high NaCl concentrations. Calcium levels in the 9.0 dS·m−1 treatment of A. parryi (1.35%) and A. weberi (1.44%) were noticeably lower than of Agave spp. (4.16%) evaluated by Nobel and Berry (1985). Even in the control treatments, the Ca levels were still fairly low for A. parryi (2.75%) and A. weberi (2.87%) as compared with that reported by Nobel and Berry (1985). However, Lock (1962) reported that mature leaves of field-grown A. sisalana in Tanzania had similar levels of Ca (1.4%), indicating that not all Agave need high Ca concentrations in their leaves to be productive. Furthermore, seedlings of A. deserti did not vary in growth with Ca levels ranging from 0.0008% to 0.02% (Nobel and Berry, 1985). Agave plants have been found to grow in soil Ca levels ranging from 0.015% to 0.01% (Nobel and Berry, 1985).

Although decreases of K and P were statistically significant in A. parryi, their low concentrations (1.97% K, 0.40% P) were still above the average values found by Nobel and Berry (1985). Furthermore, the lowest S concentrations in A. parryi (0.19%) and A. weberi (0.25%) were above that found in well watered and fertilized A. angustifolia (Ruiz-Luna et al., 2011). Despite the decrease in Mg and Mn in both A. parryi and A. weberi, the lowest Mg levels in A. parryi (0.52%) and A. weberi (0.55%) were relatively similar to the average of the six Agave spp. mentioned above (0.55%) (Nobel and Berry, 1985). Also, Mn levels in the highest NaCl treatments of A. parryi (65 ppm) and A. weberi (39 ppm) were considerably larger compared with the average (18 ppm) of the six species evaluated by Nobel and Berry (1985). Studies on micronutrient deficiency symptoms in A. sisalana indicated that deficiencies occurred below ≈10 ppm Mn, 2 ppm Cu, and 5 ppm Zn (Lock, 1962; Pinkerton, 1971). The plants in our study thus appeared not to have experienced micronutrient deficiencies. Despite a decrease in nutrient uptake at higher salt concentrations, actual physiological impairment to the plants appeared to be minimal, which is interesting considering that Na levels increased in both A. parryi and A. weberi plants as salt treatments increased (Table 3). These data corroborate with that observed by Schuch and Kelly (2008), but we do not know to what degree the plants may have excluded Na from their tissues, if at all. The presence of such a tolerance mechanism in agaves needs to be further explored.

The relations between salinity and mineral nutrition are extremely complex (Grattan and Grieve, 1999). Such complexity makes it difficult to predict which nutrients would be deficient in agaves growing in saline soils. Based on studies of other plants, it is common for most essential elements to decrease as salinity increases (Parida and Das, 2005). However, whether increased salinity leads to decreases in plant growth and productivity depends on the nutrient in question, salinity level, salt composition, plant species, and environmental factors (Grattan and Grieve, 1999). Agave parryi and A. weberi responded comparatively well to high concentrations of salinity, but to identify specific nutrient deficiency threshold levels for each species, long-term experiments need to be carried out evaluating each essential nutrient separately.

Conclusions

Based on the results of our study, it appears that several Agave spp. show variation in response to high levels of salinity. However, age and stage of development may play a factor in the degree of tolerance expressed. Agave utahensis seedlings were very sensitive to high levels of salinity, with growth and survival greatly decreasing in higher salinity treatments. In contrast, A. parryi and A. weberi plants were relatively tolerant to high levels of salinity. Consequently, both species show potential to be grown in saline soils in semiarid regions as crops. Additional work, however, needs to be done to determine their degree of establishment and productivity under field conditions.

Literature Cited

  • AbrolI.YadavJ.S.P.MassoudF.1988Salt-affected soils and their management. FAO Rome

  • Al-RawahyS.A.StroehleinJ.L.PessarakliM.1992Dry-matter yield and nitrogen-15, Na+, Cl-, and K+ content of tomatoes under sodium-chloride stressJ. Plant Nutr.15341358

    • Search Google Scholar
    • Export Citation
  • AyersR.S.WestcotD.W.1985Water quality for agriculture. FAO Rome

  • BaldwinB.G.GoldmanD.H.KeilD.J.PattersonR.RosattiT.J.WilkenD.H.2012The Jepson manual: Vascular plants of California. University of California Press Berkeley CA

  • BohnH.L.McNealB.L.O’ConnorG.A.1985Soil chemistry. Wiley New York NY

  • BorlandA.M.GriffithsH.HartwellJ.SmithJ.A.C.2009Exploiting the potential of plants with crassulacean acid metabolism for bioenergy production on marginal landsJ. Expt. Bot.6028792896

    • Search Google Scholar
    • Export Citation
  • BouslamaM.SchapaughW.T.1984Stress tolerance in soybeans. I. Evaluation of three screening techniques for heat and drought toleranceCrop Sci.24933937

    • Search Google Scholar
    • Export Citation
  • CastetterE.F.BellW.H.GroveA.R.1938The early utilization and the distribution of agave in the American southwest. University of New Mexico Press Albuquerque NM

  • ConluR.HaD.ShenJ.2011Exploring the potential of Agave as a biofuel crop on arid land. University of Nevada Las Vegas NV. 18 Dec. 2015. <http://digitalscholarship.unlv.edu/focs_ug_research/2011/april16/30/>

  • DavisS.C.DohlemanF.G.LongS.P.2011The global potential for Agave as a biofuel feedstockGlob. Change Biol. Bioenergy36878

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    • Search Google Scholar
    • Export Citation
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  • El-GamassyA.El-RahmanA.A.HassibM.MandourM.1974Vegetative patterns and water economy of Agave sisalana in saline soilsZeitschrift fuer Acker-und Pflanzenbau139165171

    • Search Google Scholar
    • Export Citation
  • eMonocot Team2012Agave weberi J.F.Cels ex J.Poiss. 11 June 2015. <http://e-monocot.org/taxon/urn:kew.org:wcs:taxon:294351>

  • Escamilla-TrevinoL.L.2012Potential of plants from the genus Agave as bioenergy cropsBioEnergy Res.519

  • FeiginA.PressmanE.ImasP.MiltauO.1991Combined effects of KNO3 and salinity on yield and chemical composition of lettuce and Chinese cabbageIrr. Sci.12223230

    • Search Google Scholar
    • Export Citation
  • GentryH.S.1982Agaves of continental North America. The University of Arizona Press Tucson AZ

  • GrattanS.R.GrieveC.M.1999Salinity mineral nutrient relations in horticultural cropsSci. Hort.78127157

  • GriffithsH.1988Crassulacean acid metabolism: A re-appraisal of physiological plasticity in form and functionAdv. Bot. Res.154392

  • HaraY.1992Physical and chemical soil properties affecting the growth habits of Agave species. Masters of Science University of Arizona Tucson AZ

  • HeatonE.A.DohlemanF.G.LongS.P.2008Meeting US biofuel goals with less land: The potential of MiscanthusGlob. Change Biol.1420002014

  • HoltumJ.A.M.ChambersD.MorganT.TanD.K.Y.2011Agave as a biofuel feedstock in AustraliaGlob. Change Biol. Bioenergy35867

  • HothornT.BretzF.WestfallP.2008Simultaneous inference in general parametric modelsBiometrical J.50346363

  • IrishM.IrishG.2000Agaves yuccas and related plants: A gardener’s guide. Timber Press Portland OR

  • KaterjiN.vanHoornJ.W.HamdyA.KaramF.MastrorilliM.1996Effect of salinity on water stress, growth, and yield of maize and sunflowerAgr. Water Mgt.30237249

    • Search Google Scholar
    • Export Citation
  • KaterjiN.van HoornJ.W.HamdyA.MastrorilliM.KaramF.1998Salinity and drought, a comparison of their effects on the relationship between yield and evapotranspirationAgr. Water Mgt.364554

    • Search Google Scholar
    • Export Citation
  • KhanM.A.UngarI.A.ShowalterA.M.1999Effects of salinity on growth, ion content, and osmotic relations in Halopyrum mucronatum (L.) StapfJ. Plant Nutr.22191204

    • Search Google Scholar
    • Export Citation
  • KonikowL.F.2013Groundwater depletion in the United States (1900−2008). U.S. Geological Survey Scientific Investigations Report 2013−5079. United States Geological Survey Washington DC. 18 Dec. 2015. <http://pubs.usgs.gov/sir/2013/5079>

  • LockG.W.1962Sisal: Twenty-five years’ sisal research. Longmans London

  • MaksimovicI.IlinŽ.2012Effects of salinity on vegetable growth and nutrients uptake p. 169–187. In: T.S. Lee (ed.). Irrigation systems and practices in challenging environments. InTech Rijeka Croatia

  • MassoudF.1976Basic principles for prognosis and monitoring of salinity and sodicity. Proc. Intl. Salinity Conf. Lubbock TX

  • MinnisP.E.PlogS.E.1976A study of the site specific distribution of Agave parryi in east central ArizonaKiva41299308

  • MiyamotoS.2008Salt tolerance of landscape plants common to the Southwest. Texas Water Resources Institute El Paso TX

  • MoghbeliE.FathollahiS.SalariH.AhmadiG.SaliqehdarF.SafariA.GrouhM.S.H.2012Effects of salinity stress on growth and yield of Aloe vera LJ. Med. Plants Res.632723277

    • Search Google Scholar
    • Export Citation
  • MunnsR.JamesR.2003Screening methods for salinity tolerance: A case study with tetraploid wheatPlant Soil253201218

  • MunnsR.TesterM.2008Mechanisms of salinity toleranceAnnu. Rev. Plant Biol.59651681

  • NerdA.KaradiA.MizrahiY.1991Salt tolerance of prickly pear cactus (Opuntia ficus-indica)Plant Soil137201207

  • NicholsB.A.HopkinsB.G.JolleyV.D.WebbB.L.GreenwoodB.G.BuckJ.R.2012Phosphorus and zinc interactions and their relationships with other nutrients in maize grown in chelator-buffered nutrient solutionJ. Plant Nutr.35123141

    • Search Google Scholar
    • Export Citation
  • NobelP.S.1984PAR and temperature influences on CO2 uptake by desert CAM plantsAdv. Photosyn. Res.3193200

  • NobelP.S.1991Achievable productivities of certain CAM plants: Basis for high values compared with C3 and C4 plantsNew Phytol.119183205

  • NobelP.S.1994Remarkable agaves and cacti. Oxford University Press New York NY

  • NobelP.S.1996Responses of some North American CAM plants to freezing temperatures and doubled CO2 concentrations: Implications of global climate change for extending cultivationJ. Arid Environ.34187196

    • Search Google Scholar
    • Export Citation
  • NobelP.S.2010Desert wisdom/agaves and cacti: CO2 water climate change. iUniverse New York NY

  • NobelP.S.BerryW.L.1985Element responses of agavesAmer. J. Bot.72686694

  • NobelP.S.SmithS.D.1983High and low-temperature tolerances and their relationships to distribution of agavesPlant Cell Environ.6711719

  • NunezH.M.RodriguezL.F.KhannaM.2011Agave for tequila and biofuels: An economic assessment and potential opportunitiesGlob. Change Biol. Bioenergy34357

    • Search Google Scholar
    • Export Citation
  • ParidaA.K.DasA.B.2005Salt tolerance and salinity effects on plants: A reviewEcotoxicol. Environ. Saf.60324349

  • Peña-ValdiviaC.B.Sánchez-UrdanetaA.B.2009Effects of substrate water potential in root growth of Agave salmiana Otto ex Salm-Dyck seedlingsBiol. Res.42239248

    • Search Google Scholar
    • Export Citation
  • PessarakliM.1991Dry-matter yield, N-15 absorption, and water-uptake by green bean under sodium-chloride stressCrop Sci.3116331640

  • PinkertonA.1971Some micronutrient deficiencies in sisal (Agave sisalana)Exp. Agr.7113122

  • Ruiz-LunaJ.Velasco-VelascoV.Maldonado-PeraltaR.Enríquez-del ValleJ.Campos-ÁngelesG.Rodríguez-OrtizG.Preciado-RangelP.2011Expression of nutrient deficiencies of nitrogen, phosphorus, potassium, sulfur and iron in Agave angustifolia HawActa Hort.947339345

    • Search Google Scholar
    • Export Citation
  • SchuchU.K.KellyJ.J.2008Salinity tolerance of cacti and succulents. College of Agriculture and Life Sciences University of Arizona Tucson AZ. 18 Dec. 2015. <http://hdl.handle.net/10150/216639>

  • ShaheenR.Hood-NowotnyR.C.2005Carbon isotope discrimination: Potential for screening salinity tolerance in rice at the seedling stage using hydroponicsPlant Breed.124220224

    • Search Google Scholar
    • Export Citation
  • SteinbergR.A.1953Symptoms of molybdenum deficiency in tobaccoPlant Physiol.28319322

  • WadaY.van BeekL.P.H.van KempenC.M.ReckmanJ.W.T.M.VasakS.BierkensM.F.P.2010Global depletion of groundwater resourcesGeophys. Res. Lett.37L20402

    • Search Google Scholar
    • Export Citation
  • WelshS.L.AtwoodN.D.GoodrichS.HigginsL.C.1993A Utah flora. Brigham Young University Provo UT

  • WinterK.SmithJ.A.C.1996An introduction to crassulacean acid metabolism. Biochemical principles and ecological diversity p. 1–13. In: K. Winter and J.A.C. Smith (eds.). Crassulacean acid metabolism. Springer Berlin Heidelberg Germany

  • YangX.CushmanJ.C.BorlandA.M.EdwardsE.J.WullschlegerS.D.TuskanG.A.OwenN.A.GriffithsH.SmithJ.A.C.De PaoliH.C.WestonD.J.CottinghamR.HartwellJ.DavisS.C.SilveraK.MingR.SchlauchK.AbrahamP.StewartJ.R.GuoH.-B.AlbionR.HaJ.LimS.D.WoneB.W.M.YimW.C.GarciaT.MayerJ.A.PetereitJ.NairS.S.CaseyE.HettichR.L.CeustersJ.RanjanP.PallaK.J.YinH.Reyes-GarciaC.AndradeJ.L.FreschiL.BeltranJ.D.DeverL.V.BoxallS.F.WallerJ.DaviesJ.BupphadaP.KaduN.WinterK.SageR.F.AguilarC.N.SchmutzJ.JenkinsJ.HoltumJ.A.M.2015A roadmap for research on crassulacean acid metabolism (CAM) to enhance sustainable food and bioenergy production in a hotter, drier worldNew Phytol.207491504

    • Search Google Scholar
    • Export Citation

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Contributor Notes

We are thankful to three BYU undergraduate students, Cali Mc Murtrey, Yue Shen, and Westen Archibald, for helping us carry out this experiment.

Corresponding author. E-mail: rstewart@byu.edu.

  • AbrolI.YadavJ.S.P.MassoudF.1988Salt-affected soils and their management. FAO Rome

  • Al-RawahyS.A.StroehleinJ.L.PessarakliM.1992Dry-matter yield and nitrogen-15, Na+, Cl-, and K+ content of tomatoes under sodium-chloride stressJ. Plant Nutr.15341358

    • Search Google Scholar
    • Export Citation
  • AyersR.S.WestcotD.W.1985Water quality for agriculture. FAO Rome

  • BaldwinB.G.GoldmanD.H.KeilD.J.PattersonR.RosattiT.J.WilkenD.H.2012The Jepson manual: Vascular plants of California. University of California Press Berkeley CA

  • BohnH.L.McNealB.L.O’ConnorG.A.1985Soil chemistry. Wiley New York NY

  • BorlandA.M.GriffithsH.HartwellJ.SmithJ.A.C.2009Exploiting the potential of plants with crassulacean acid metabolism for bioenergy production on marginal landsJ. Expt. Bot.6028792896

    • Search Google Scholar
    • Export Citation
  • BouslamaM.SchapaughW.T.1984Stress tolerance in soybeans. I. Evaluation of three screening techniques for heat and drought toleranceCrop Sci.24933937

    • Search Google Scholar
    • Export Citation
  • CastetterE.F.BellW.H.GroveA.R.1938The early utilization and the distribution of agave in the American southwest. University of New Mexico Press Albuquerque NM

  • ConluR.HaD.ShenJ.2011Exploring the potential of Agave as a biofuel crop on arid land. University of Nevada Las Vegas NV. 18 Dec. 2015. <http://digitalscholarship.unlv.edu/focs_ug_research/2011/april16/30/>

  • DavisS.C.DohlemanF.G.LongS.P.2011The global potential for Agave as a biofuel feedstockGlob. Change Biol. Bioenergy36878

  • DohlemanF.G.LongS.P.2009More productive than maize in the Midwest: How does Miscanthus do it?Plant Physiol.15021042115

  • Dominguez-FausR.PowersS.E.BurkenJ.G.AlvarezP.J.2009The water footprint of biofuels: A drink or drive issue?Environ. Sci. Technol.4330053010

    • Search Google Scholar
    • Export Citation
  • El-BagouryO.El-AgroudyM.ShenoudaM.1993Effect of salinity levels on growth of six plant speciesEgypt. J. Agron.18129143

  • El-GamassyA.El-RahmanA.A.HassibM.MandourM.1974Vegetative patterns and water economy of Agave sisalana in saline soilsZeitschrift fuer Acker-und Pflanzenbau139165171

    • Search Google Scholar
    • Export Citation
  • eMonocot Team2012Agave weberi J.F.Cels ex J.Poiss. 11 June 2015. <http://e-monocot.org/taxon/urn:kew.org:wcs:taxon:294351>

  • Escamilla-TrevinoL.L.2012Potential of plants from the genus Agave as bioenergy cropsBioEnergy Res.519

  • FeiginA.PressmanE.ImasP.MiltauO.1991Combined effects of KNO3 and salinity on yield and chemical composition of lettuce and Chinese cabbageIrr. Sci.12223230

    • Search Google Scholar
    • Export Citation
  • GentryH.S.1982Agaves of continental North America. The University of Arizona Press Tucson AZ

  • GrattanS.R.GrieveC.M.1999Salinity mineral nutrient relations in horticultural cropsSci. Hort.78127157

  • GriffithsH.1988Crassulacean acid metabolism: A re-appraisal of physiological plasticity in form and functionAdv. Bot. Res.154392

  • HaraY.1992Physical and chemical soil properties affecting the growth habits of Agave species. Masters of Science University of Arizona Tucson AZ

  • HeatonE.A.DohlemanF.G.LongS.P.2008Meeting US biofuel goals with less land: The potential of MiscanthusGlob. Change Biol.1420002014

  • HoltumJ.A.M.ChambersD.MorganT.TanD.K.Y.2011Agave as a biofuel feedstock in AustraliaGlob. Change Biol. Bioenergy35867

  • HothornT.BretzF.WestfallP.2008Simultaneous inference in general parametric modelsBiometrical J.50346363

  • IrishM.IrishG.2000Agaves yuccas and related plants: A gardener’s guide. Timber Press Portland OR

  • KaterjiN.vanHoornJ.W.HamdyA.KaramF.MastrorilliM.1996Effect of salinity on water stress, growth, and yield of maize and sunflowerAgr. Water Mgt.30237249

    • Search Google Scholar
    • Export Citation
  • KaterjiN.van HoornJ.W.HamdyA.MastrorilliM.KaramF.1998Salinity and drought, a comparison of their effects on the relationship between yield and evapotranspirationAgr. Water Mgt.364554

    • Search Google Scholar
    • Export Citation
  • KhanM.A.UngarI.A.ShowalterA.M.1999Effects of salinity on growth, ion content, and osmotic relations in Halopyrum mucronatum (L.) StapfJ. Plant Nutr.22191204

    • Search Google Scholar
    • Export Citation
  • KonikowL.F.2013Groundwater depletion in the United States (1900−2008). U.S. Geological Survey Scientific Investigations Report 2013−5079. United States Geological Survey Washington DC. 18 Dec. 2015. <http://pubs.usgs.gov/sir/2013/5079>

  • LockG.W.1962Sisal: Twenty-five years’ sisal research. Longmans London

  • MaksimovicI.IlinŽ.2012Effects of salinity on vegetable growth and nutrients uptake p. 169–187. In: T.S. Lee (ed.). Irrigation systems and practices in challenging environments. InTech Rijeka Croatia

  • MassoudF.1976Basic principles for prognosis and monitoring of salinity and sodicity. Proc. Intl. Salinity Conf. Lubbock TX

  • MinnisP.E.PlogS.E.1976A study of the site specific distribution of Agave parryi in east central ArizonaKiva41299308

  • MiyamotoS.2008Salt tolerance of landscape plants common to the Southwest. Texas Water Resources Institute El Paso TX

  • MoghbeliE.FathollahiS.SalariH.AhmadiG.SaliqehdarF.SafariA.GrouhM.S.H.2012Effects of salinity stress on growth and yield of Aloe vera LJ. Med. Plants Res.632723277

    • Search Google Scholar
    • Export Citation
  • MunnsR.JamesR.2003Screening methods for salinity tolerance: A case study with tetraploid wheatPlant Soil253201218

  • MunnsR.TesterM.2008Mechanisms of salinity toleranceAnnu. Rev. Plant Biol.59651681

  • NerdA.KaradiA.MizrahiY.1991Salt tolerance of prickly pear cactus (Opuntia ficus-indica)Plant Soil137201207

  • NicholsB.A.HopkinsB.G.JolleyV.D.WebbB.L.GreenwoodB.G.BuckJ.R.2012Phosphorus and zinc interactions and their relationships with other nutrients in maize grown in chelator-buffered nutrient solutionJ. Plant Nutr.35123141

    • Search Google Scholar
    • Export Citation
  • NobelP.S.1984PAR and temperature influences on CO2 uptake by desert CAM plantsAdv. Photosyn. Res.3193200

  • NobelP.S.1991Achievable productivities of certain CAM plants: Basis for high values compared with C3 and C4 plantsNew Phytol.119183205

  • NobelP.S.1994Remarkable agaves and cacti. Oxford University Press New York NY

  • NobelP.S.1996Responses of some North American CAM plants to freezing temperatures and doubled CO2 concentrations: Implications of global climate change for extending cultivationJ. Arid Environ.34187196

    • Search Google Scholar
    • Export Citation
  • NobelP.S.2010Desert wisdom/agaves and cacti: CO2 water climate change. iUniverse New York NY

  • NobelP.S.BerryW.L.1985Element responses of agavesAmer. J. Bot.72686694

  • NobelP.S.SmithS.D.1983High and low-temperature tolerances and their relationships to distribution of agavesPlant Cell Environ.6711719

  • NunezH.M.RodriguezL.F.KhannaM.2011Agave for tequila and biofuels: An economic assessment and potential opportunitiesGlob. Change Biol. Bioenergy34357

    • Search Google Scholar
    • Export Citation
  • ParidaA.K.DasA.B.2005Salt tolerance and salinity effects on plants: A reviewEcotoxicol. Environ. Saf.60324349

  • Peña-ValdiviaC.B.Sánchez-UrdanetaA.B.2009Effects of substrate water potential in root growth of Agave salmiana Otto ex Salm-Dyck seedlingsBiol. Res.42239248

    • Search Google Scholar
    • Export Citation
  • PessarakliM.1991Dry-matter yield, N-15 absorption, and water-uptake by green bean under sodium-chloride stressCrop Sci.3116331640

  • PinkertonA.1971Some micronutrient deficiencies in sisal (Agave sisalana)Exp. Agr.7113122

  • Ruiz-LunaJ.Velasco-VelascoV.Maldonado-PeraltaR.Enríquez-del ValleJ.Campos-ÁngelesG.Rodríguez-OrtizG.Preciado-RangelP.2011Expression of nutrient deficiencies of nitrogen, phosphorus, potassium, sulfur and iron in Agave angustifolia HawActa Hort.947339345

    • Search Google Scholar
    • Export Citation
  • SchuchU.K.KellyJ.J.2008Salinity tolerance of cacti and succulents. College of Agriculture and Life Sciences University of Arizona Tucson AZ. 18 Dec. 2015. <http://hdl.handle.net/10150/216639>

  • ShaheenR.Hood-NowotnyR.C.2005Carbon isotope discrimination: Potential for screening salinity tolerance in rice at the seedling stage using hydroponicsPlant Breed.124220224

    • Search Google Scholar
    • Export Citation
  • SteinbergR.A.1953Symptoms of molybdenum deficiency in tobaccoPlant Physiol.28319322

  • WadaY.van BeekL.P.H.van KempenC.M.ReckmanJ.W.T.M.VasakS.BierkensM.F.P.2010Global depletion of groundwater resourcesGeophys. Res. Lett.37L20402

    • Search Google Scholar
    • Export Citation
  • WelshS.L.AtwoodN.D.GoodrichS.HigginsL.C.1993A Utah flora. Brigham Young University Provo UT

  • WinterK.SmithJ.A.C.1996An introduction to crassulacean acid metabolism. Biochemical principles and ecological diversity p. 1–13. In: K. Winter and J.A.C. Smith (eds.). Crassulacean acid metabolism. Springer Berlin Heidelberg Germany

  • YangX.CushmanJ.C.BorlandA.M.EdwardsE.J.WullschlegerS.D.TuskanG.A.OwenN.A.GriffithsH.SmithJ.A.C.De PaoliH.C.WestonD.J.CottinghamR.HartwellJ.DavisS.C.SilveraK.MingR.SchlauchK.AbrahamP.StewartJ.R.GuoH.-B.AlbionR.HaJ.LimS.D.WoneB.W.M.YimW.C.GarciaT.MayerJ.A.PetereitJ.NairS.S.CaseyE.HettichR.L.CeustersJ.RanjanP.PallaK.J.YinH.Reyes-GarciaC.AndradeJ.L.FreschiL.BeltranJ.D.DeverL.V.BoxallS.F.WallerJ.DaviesJ.BupphadaP.KaduN.WinterK.SageR.F.AguilarC.N.SchmutzJ.JenkinsJ.HoltumJ.A.M.2015A roadmap for research on crassulacean acid metabolism (CAM) to enhance sustainable food and bioenergy production in a hotter, drier worldNew Phytol.207491504

    • Search Google Scholar
    • Export Citation
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