Sustainability 10 03083
Sustainability 10 03083
Sustainability 10 03083
Article
Reclamation of Saline–Sodic Soils with Combined
Amendments: Impact on Quinoa Performance and
Biological Soil Quality
María Alcívar 1 , Andrés Zurita-Silva 2 ID
, Marco Sandoval 1 , Cristina Muñoz 1
and Mauricio Schoebitz 1, * ID
1 Department of Soils and Natural Resources, Faculty of Agronomy, Universidad de Concepción,
Campus Chillan, Avenida Vicente Méndez 595, Chillán, Chile; [email protected] (M.A.);
[email protected] (M.S.); [email protected] (C.M.)
2 Instituto de Investigaciones Agropecuarias, (INIA), Centro de Investigación Intihuasi,
Colina San Joaquin s/n, La Serena, Coquimbo, Chile; [email protected]
* Correspondence: [email protected]; Tel.: +56-41-2661438
Received: 17 July 2018; Accepted: 14 August 2018; Published: 30 August 2018
Abstract: The objective of this study was to evaluate the individual and synergic effects of
the application of Biochar (B), Humic Substances (HS), and Gypsum (G) on the soil properties
of a saline–sodic soil, and plant growth and seed quality (polyphenols, protein and yield) of
quinoa. Treatments included (B) 22 t ha−1 , (HS) 5 kg ha−1 , and (G) 47.7 t ha−1 . Two quinoa
genotypes from Arid Zones (AZ-51 and AZ-103) were selected and established in eight treatments.
The B + HS + G combined treatment resulted in increases in root biomass of 206% and 176% in
AZ-51 and AZ-103, respectively. Furthermore, electrical conductivity (ECe), sodium adsorption
ratio (SAR), and exchangeable sodium percentage (ESP) decreased significantly in all treated soils.
When compared to the control, ESP decreased 11-fold in the G treatment, and 9–13-fold in the B + G;
B + HS; and B + HS + G treatments. Similarly, soil microbial biomass increased 112% and 322% in the
B + HS + G treatment in AZ-51 and AZ-103 genotypes, respectively. Therefore, it can be concluded
that the application of combined amendments (B + HS + G) represents an alternative for reclaiming
degraded soils, including saline–sodic soils.
1. Introduction
Soil degradation resulting from salinity and sodicity is a major environmental threat to soil
fertility and agricultural productivity in arid and semiarid regions of the world [1]. Saline–sodic
soils are degraded due to the simultaneous effect of salinity and sodicity. This causes loss of
soil physical structure by clay swelling, and dispersion because of high Na+ concentrations in the
soil solution or at the exchange phase [2]. Apart from these physicochemical effects, this leads to
biological properties, such as microbial respiration and biomass, becoming worse [3]. On the other
hand, salinity affects plant growth by creating osmotic imbalances and specific ion toxicities [4],
which pose limitations to morphological, histological, chemical, biochemical, and metabolic processes.
In turn, these reduce stomatal opening and photosynthetic rate, leading to decreased plant growth,
crop yield, and quality [4,5]. Agricultural adaptation to changing climatic conditions, expected to
entail increasing soil salinization, relies on the use of crops that can tolerance abiotic and biotic
stresses [6]. In this sense, quinoa (Chenopodium quinoa Willd.) has been considered for agricultural
diversification due to its extraordinary adaptability to various environmental stresses, such as soil
salinity, low temperature, drought, and nutrient-poor soils [7]. In the last decades, quinoa has
attracted the attention of researchers and consumers worldwide for being one of food plants with the
highest content of essential aminoacids, vitamins, phenolic compounds, and minerals [8]. However,
high salinity can negatively influence root length, chlorophyll content, plant growth, as well as seed
yield [6,9]. According to Ramzani et al. [10], salt-affected soils influence the nutritional quality of quinoa
seeds so that protein content decreases, whereas polyphenol levels increase. Therefore, a successful
reclamation of saline–sodic soils is of great importance for crop productivity [11], and a key factor in
addressing the world’s food security challenges [12]. Reclamation of saline–sodic soils requires the
removal of sodium from the soil exchange sites by divalent cations (preferably Ca2+ ) to promote soil
flocculation. The most common amendment source can be calcium, which provides soluble calcium
within the soil. The replaced Na+ is removed either below root zone or out of the soil profile by leaching
water [13]. Gypsum is the most commonly applied product for the reclamation of saline–sodic soils
and can improve physical and chemical soil properties primarily by maintaining a favorable electrolyte
concentration in soil solution. As adsorbed Na+ on exchangeable sites of clay particles are considered
to be responsible for soil dispersion, gypsum can prevent it by maintaining high Ca/Na ratios, and thus
promoting clay flocculation and structure stability [14]. On the other hand, organic amendments can
increase dissolution of native calcite (CaCO3 ) minerals via increased formation of carbonic acid in
the soil profile, thus dissolution could release Ca2+ in the soil solution to facilitate the removal of
Na+ from cation exchange sites [15]. Therefore, the addition of organic matter also represents an
alternative for reclaiming a variety of degraded soils, including salt-affected soils. In fact, significant
improvements have been reported regarding soil physical, chemical, and biological characteristics with
the use of organic matter [16]. Gupta et al. Ref. [17] found that the combined application of gypsum
and organic amendments in sodic soils improved soil properties, resulting in decreased soil bulk
density, electrical conductivity (EC), and exchangeable sodium percentage (ESP), but also in increased
soil biological activity. Humic substances are widely recognized as key components of soil fertility
because they control the physicochemical and biological properties of the rhizosphere, perform various
functions in the soil and regulate plant growth. In fact, humic substances improve soil properties,
such as aggregation, aeration, and water holding capacity [18,19]. Furthermore, Ciarkowska et al. [20]
reported that humic substances applied to the soil contributed substantially to improve soil quality
status, resulting in increased organic carbon, enzymatic activity, root biomass, and yield. Biochar
is another soil amendment [21] that can improve soil physical conditions. It is more recalcitrant
than humic substances and less likely to directly support microbial growth, but it can significantly
promote soil biological activity due to the release of temporary labile pyrolysis products [22]; however,
this effect could be very temporary [23]. Salt-affected soils can benefit from biochar application by
increased contents of soil organic carbon and nutrients (K+ , Ca2+ , Mg2+ , Zn, Mn), increased surface
area, enhanced physical properties by balancing water content and air porosity, increased retention of
polyvalent cations, and replacement of Na+ from exchange sites by providing Ca2+ in soil solution [24].
In this sense, the addition of organic amendments in combination with gypsum has proven successful
in reducing adverse effects on soil properties associated with a high content of sodium. However, there
is no information about the synergistic effects between biochar, humic substances, and gypsum on the
reclamation of saline–sodic soils and their impact on quinoa crop growth. The objectives of this study
were: (a) to evaluate changes in the chemical and biological characteristics of saline–sodic soil after the
application of combined amendments B, HS, G; (b) to evaluate the effects of these amendments on
the physiology, productivity, and seed quality of two quinoa genotypes. The hypothesis tested in this
work was that the combined application of amendments enhances chemical and biological properties
of saline–sodic soils, and that this effect on soil properties could in turn result on a significant impact
on quinoa performance.
Sustainability 2018, 10, 3083 3 of 17
2.4. Leaching
Leaching was applied before seedlings were planted to decrease the high salinity of the soil.
It consisted in partially adding tap water for thirty days, applying 15 l pot−1 . The soil electrical
conductivity post leaching was 15 dS m−1 . Soil leaching is an agricultural practice commonly used in
Huasco in order to reduce soil salinity to levels that crop to be grown can tolerate. The average ECe
value for Huasco soils is 17 dS m−1 [27].
2.5. Amendments
Pine-woodchip biochar and humic substances were used as organic amendments, while gypsum
was used as an inorganic amendment. Biochar was produced by slow pyrolysis at 450◦ C for 30 min
and then cool to room temperature for 60 min. Processing of carbonaceous material was carried at
the UDT (Technology Unit of the University of Concepción - Chile). Some properties of biochar are
presented below: total carbon (C %) 46; total nitrogen (N %) 0.5; C:N ratio 98.5; total Ca – Mg (%):
0.8 – 0.12 [28]. Biosolve (Oiko, Chile) product containing 70% humic acids, 15% fulvic acids, and 10%
K2 O was used as source of humic substances derived from leonardite. Gypsum was obtained from the
local market, with a composition of SO4 16–18%, CaO 23–24%.
The gypsum requirement of the soil was determined using the following equation [29]:
where GR is the net gypsum requirement of the soil (t ha−1 ); ESPi is the initial exchangeable sodium
percentage; ESPf is the final exchangeable sodium percentage; CEC is the cation exchangeable
capacity (cmol kg−1 ); SD is the soil depth (cm); BD is bulk density (g cm−3 ); and F is the Ca-Na
exchange efficiency.
To reduce initial soil ESP from 58% to 45%, 47.7 t ha−1 of GR was used.
2.9. Chemical and Biological Soil Analysis, and Leaf Tissue Analysis
Chemical analyses were performed measuring pH, ECe, and soluble cations (Ca2+ , Mg2+ , Na+ ) of
saturation paste following standard methods [33]. In addition, exchangeable cation concentrations
Sustainability 2018, 10, 3083 5 of 17
were measured [33]. All analyses were conducted in the ISO 17025 accredited laboratories of the
Department of Soils and Natural Resources of the University of Concepción.
ESP was calculated by the following equation where the concentrations of exchangeable cations
are expressed in cmol kg −1 :
SAR was calculated by the following equation where a chemical element symbol indicates a
concentration in meq l −1 :
Na+
SAR = p (3)
(Ca+2 + Mg+2 )/2
Microbial soil biomass activity was determined by hydrolysis of fluorescein diacetate (FDA).
For this analysis, an amount of 0.5 g of wet soil was weighed in screw cap test tubes; samples were in
triplicate and a blank was also included. Amounts of 4.95 mL of sodium phosphate buffer and 0.05 mL
of FDA were added and stirred, and then tubes were placed in a thermoregulated bath at 25 ◦ C for
1 h. Subsequently, samples were cooled in an ice bath, and a volume of 5 mL of acetone was added.
The solutions were shaken and filtered, and absorbance was read at 490 nm in a spectrophotometer
against a reagent blank [34]. Soil respiration was determined by weighing 20 g of soil (in duplicate)
per treatment, and placed in an incubation bottle. A volume of 7.5 mL of NaOH was added in a
centrifuge tube and placed in an incubation bottle. Then, bottles without soil (blank) were hermetically
closed and remained in an incubation chamber at 22 ◦ C and constant humidity for 7 days. After the
incubation time, a volume of 1mL of NaOH was taken from the centrifuge tube and mixed with a
volume of 2 mL of BaCl2 , and then the solution was titrated with HCl 0.1 M. The data were expressed
as µg CO2 -C g−1 soil oven dried (105 ◦ C) [34].
Sodium leaf analyses were performed following standard methods [35].
3. Results
3.1. Effects of the Amendments on Growth and Physiological Parameters of Quinoa Plants
One of the objectives of this research was to evaluate the effects of the application of biochar,
humic substances, and gypsum on quinoa growth. The root biomass in AZ-51 quinoa genotype showed
a significant increase of 413% in the B + HS + G treatment when compared to the control. The combined
applications of B + G; B + HS; and B + HS + G also resulted in significant increases of 57, 73, and 93%
in the root biomass of AZ-103 genotype, respectively (Table 1). In terms of root length, HS + G; B;
B + HS + G resulted in significant increases of 51, 76, and 106%, respectively, in AZ-51 compared to the
control treatment, while AZ-103 also exhibited significant increases in B; B + G; and B + HS treatments
respect to the control (Table 1).
Regarding physiological variables of quinoa, chlorophyll index (SPAD values) in AZ-51
genotype did not increase significantly with amendment applications when compared to the control
(p value = 0.1028). Despite this, the same parameter showed significant increases in AZ-103 for all
treatments compared to the control. The highest SPAD values were obtained with HS + G; G; B; B + G;
Sustainability 2018, 10, 3083 6 of 17
and B + HS, with increases of 39, 33, 32, 30, and 27%, respectively, compared to the control (Table 2).
On the other hand, amendment applications resulted in significant increases in stomatal conductance
in both quinoa genotypes. When compared to the control treatment, this parameter was significantly
higher in AZ-51 for B + HS + G; HS; B + G; G; and B + HS treatments, whereas all treatments were
significant higher in AZ-103 genotype (Table 2).
Seed yield in AZ-51 genotype presented significant increases of 116 and 85% for G and HS + G
treatments, respectively (Duncan test p > 0.05), while a similar behavior was observed in all treated
soils in AZ-103 compared to the control (Figure 1).
Table 1. Influence of chemical and organic amendments on root length and root dry weight of quinoa
genotypes grown in saline–sodic soil.
Table 2. Influence of chemical and organic amendments on the physiological parameters of quinoa
genotypes grown in saline–sodic soil.
10.00 C B
a G HS
9.00
ab B+G B + HS
8.00
Seed yield (g plant -1) HS + G B + HS + G
7.00 bc
6.00 cd
cd a
cd a
5.00 d a a a a
d a
4.00
3.00
2.00 b
1.00
0.00
AZ-51 AZ-103
Figure 1. Seed yield (g plant −1 ) of quinoa genotypes grown in saline–sodic soil in response to
Figure 1.
chemical andSeed yieldamendments.
organic (g plant -1) of Values
quinoa aregenotypes
means of grown
four in saline–sodic
replicates. soilbars
Error in response
represent to
chemical and organic amendments. Values are means of four replicates. Error
the standard error. Significance: (AZ-51 p < 0.0001); (AZ-103 p = 0.0009). Values with the samebars represent the
standard error. Significance: (AZ-51 p < 0.0001); (AZ-103 p = 0.0009). Values with the same
letter are not significantly different according to Duncan’s test (p ≤ 0.05). C = control; B = biochar; letter are
not significantly different according to Duncan’s test (p ≤ 0.05). C = control; B = biochar;
G = gypsum; HS = humic substances; B + G = biochar + gypsum; B + HS = biochar + humic substances; G = gypsum;
HSHS+G = humic
= humicsubstances;
substancesB++gypsum;
G = biochar + gypsum;
B + HS B + HS+=humic
+ G = biochar biochar + humic +substances;
substances gypsum. HS + G =
humic substances + gypsum; B + HS + G = biochar + humic substances + gypsum.
3.2. Polyphenols and Protein Content in Quinoa Seeds
3.2 Polyphenols and Protein Content in quinoa seeds
Total polyphenol content (GAE) did not show significant differences (p value = 0.2239) between
Totalinpolyphenol
treatments contentcompared
AZ-51 genotype (GAE) didtonot
theshow significant
control. differences
Nevertheless, (p valuedifferences
significant = 0.2239) between
were
found in AZ-103, with a 28% decrease in GAE concentration in the B + HS + G treatment comparedwere
treatments in AZ-51 genotype compared to the control. Nevertheless, significant differences to
found
the in AZ-103,
control (Table 3).with a 28% decrease in GAE concentration in the B + HS + G treatment compared to
theProtein
controlcontent
(Table 3).
in seeds of AZ-51 genotype recorded significant increases of 45, 34, 29, and 26% in
Protein content
HS; HS + G; B + HS; and in B
seeds
+ HSof+AZ-51 genotype
G treatments, recorded significant
respectively. increases
This parameter of 45, an
recorded 34,increase
29, and 26%
of
23% in the biochar treatment in seeds of AZ-103 genotype compared to the control (Table 3).an increase
in HS; HS + G; B + HS; and B + HS + G treatments, respectively. This parameter recorded
of 23% in the biochar treatment in seeds of AZ-103 genotype compared to the control (Table 3).
Table 3. Contents of polyphenols (Gallic Acid Equivalent, GAE) and protein in quinoa seeds.
Table 3. Contents of polyphenols (Gallic Acid Equivalent, GAE) and protein in quinoa seeds.
Polyphenols (GAE mg −1 Protein (%)
Treatments Polyphenols (GAE mg g-1g) ) Protein (%)
Treatments AZ-51 AZ-103 AZ-51 AZ-103
AZ-51 AZ-103 AZ-51 AZ-103
C C 1.02 ± a0.08 a 1.2±0.07
1.02±0.08 1.2 ± 0.07
ab ab 9.3 ± 0.72
9.3±0.72 dd 11.4 ± 0.27 bb
11.4±0.27
B 0.75 ± 0.06 a 1.05 ± 0.09 bc 11.1 ± 0.61 bcd 14.0 ± 0.53 a
B G 0.75±0.06
0.91 ± a0.06 a 1.05±0.09
1.22 ± 0.14bc ab 11.1±0.61 bcdcd
10.4 ± 0.82 14.0±0.53
10.8 ± 0.19 ab
G HS 0.71 ± a0.03 a 1.22±0.14
0.91±0.06 1.02 ± 0.09 13.5 ± 0.26
ab bc 10.4±0.82 cd a 10.3 ± 0.48 bb
10.8±0.19
B+G 0.81 ± 0.16 a 1.38 ± 0.11 a 10.7 ± 0.76 bcd 11.9 ± 0.37 b
HS B + HS 0.71±0.03
0.87 ± a0.12 a 1.02±0.09
1.21 ± 0.11bc ab 13.5±0.26
12.0 ± 0.10aabc 10.3±0.48
11.3 ± 0.70 bb
B + GHS + G 0.81±0.16 0.78 ± a0.15 a 1.38±0.11
1.12 ± 0.09 12.5 ± 0.44
a abc 10.7±0.76 bcdab 11.8 ± 0.92 bb
11.9±0.37
B+ HS + G 0.73 ± 0.05 a 0.87 ± 0.08 c 11.8 ± 0.50 abc 11.3 ± 0.37 b
B + HS (p-value)
0.87±0.12 a
0.2239
1.21±0.11 ab
0.0137
12.0±0.10 abc
0.0018
11.3±0.70
0.0029
b
HS +areGmeans of four
Values 0.78±0.15 a Standard
replicates. 1.12±0.09
error: ± abc 12.5±0.44
. Values followed byab 11.8±0.92
the same letter in the bcolumns
do not differ significantly by Duncan’s test (p ≤ 0.05). C = control; B = biochar; G = gypsum; HS b= humic
B+ HS + G 0.73±0.05 a 0.87±0.08 c 11.8±0.50 abc 11.3±0.37
substances; B + G = biochar + gypsum; B + HS = biochar + humic substances; HS + G = humic substances + gypsum;
(p-value)
B+ 0.2239
HS + G = biochar + humic 0.0137
substances + gypsum. 0.0018 0.0029
Sustainability 2018, 10, 3083 8 of 17
3.3. Effects of Amendments on the Chemical and Biological Properties of Saline–Sodic Soils
Electrical conductivity of the saturation paste extract decreased significantly with the application
of most of the soil amendments compared to the control. Amendment applications resulted in a
significant reduction in salinity (ECe) that ranged from 33 to 46% (in AZ-51 genotype), except in
the biochar treatment. In AZ-103 genotype, ECe was also significantly lower in all treatments,
with decreases that ranged from 52 to 68% when compared to the control (Table 4).
Sodium adsorption ratio (SAR) decreased significantly in all amended soils. The maximum
decreases were obtained with gypsum (a 10.9-fold decrease on average) for individual applications,
and with B + G in case of combined treatments (a 15.2-fold decrease on average) compared to the
control (Table 4).
All treated soils recorded significantly lower soil ESP values. The largest reduction in ESP for
individual applications was observed with the G treatment, which exhibited an 11-fold reduction in
soil ESP compared to the control. In case of combined applications, the maximum decreases in ESP
were recorded in B + G; B + HS; and B + HS + G treatments, with reductions that ranged from 9- to
13-fold compared to the control treatment (Table 4).
Exchangeable Ca2+ concentrations were 40, 27, and 23% higher in G; B + HS + G; and HS + G
treatments, respectively, in AZ-51 genotype. The same treatments showed a similar trend in AZ-103
genotype. In addition, B + HS; B + G; and B treatments also resulted in significant increases in
exchangeable Ca2+ concentrations that ranged from 54 to 14% (Table 5).
Soil Exchangeable Mg2+ was significantly lower in both AZ-51 and AZ-103 with the B + G
treatment (20 and 24%, respectively) compared to the control (Table 5).
Soil Exchangeable Na+ concentrations were significantly reduced in all treated soils (Table 5).
In AZ-51genotype, exchangeable Na+ concentrations were 85% to 93% lower than the control for
combined applications; whereas values were 87% to 91% lower for individual applications. A similar
trend was observed in AZ-103 as exchangeable Na+ concentrations reduced from 82 to 92% and 81 to
89% in combined and individual applications, respectively, compared to the control.
Regarding biological soil analysis, soil and respiration microbial biomass presented significantly
increases in most of the treatments. All amended soils recorded significant increases in soil microbial
biomass compared to the control (Figure 2). Thus, the highest values for microbial biomass in both
genotypes were obtained with following treatments: B + HS + G; HS + G; B; and B + HS (ranging from
12.2 to 14.1 µg FDA g −1 soil).
Soil microbial respiration also had significant increases in most treatments (Figure 3). In AZ-51
genotype, the highest values in soil microbial respiration were observed in B + HS + G; B + G; and B,
with values 130, 88, and 85% higher, respectively, than the control. In AZ-103 genotype, all treated soils
recorded significant increases with respect to untreated soils, with values 285, 227, and 211% higher
than the control for B + HS + G; B; and HS + G treatments, respectively.
Sustainability 2018, 10, 3083 9 of 17
20
18 C B G HS B+G B + HS HS + G B + HS + G
Microbial biomass µ g F g -1 soil)
16 a a
ab a ab ab
ab
14 b
b b
12
10 c c
c
8 c d
6
4 e
2
0
AZ-51 AZ-103
20
C B G HS B+G B + HS HS + G B + HS + G
10 cd
c
8 d
6 d
4
2
0
AZ-51 AZ-103
Microbial
Figure 3.Figure respiration (µg CO - C g −1 ) in saline–sodic soil after the application of chemical
3. Microbial respiration (µ g2 CO2- C g -1) in saline–sodic soil after the application of chemical
and organic amendments.
and organic ValuesValues
amendments. are means of fourofreplicates.
are means ErrorError
four replicates. bars bars
represent the standard
represent error.
the standard
Significance:
error. (AZ-51 p < 0.0001);
Significance: (AZ-51 (AZ-103 p < (AZ-103
p < 0.0001); 0.0001). p Values withValues
< 0.0001). the samewithletter are not
the same significantly
letter are not
differentsignificantly
according different
to Duncan’s test (p
according ≤ 0.05). C
to Duncan’s test=(p
control;
≤ 0.05). B
C= biochar;
= control; B =Gbiochar;
= gypsum; HS = humic
G = gypsum; HS
substances; B +substances;
= humic G = biocharB+G + =gypsum; B + HS B= +biochar
biochar + gypsum; + humic
HS = biochar substances;
+ humic substances;HSHS ++GG==humic
humic
substances
substances + gypsum;
+ gypsum; B + HSB ++HS
G =+ G = biochar
biochar + humic
+ humic substances++ gypsum.
substances gypsum.
4. Discussion
4. Discussion
Soil salinity greatly reduces plant growth by osmotic stress, hormonal imbalance, nutrient
Soildeficiencies,
salinity greatly reduces
and specific plant growth
ion toxicity [36]. Thebyresults
osmotic stress,
obtained in hormonal
the present imbalance,
study indicate nutrient
that
deficiencies, and specific ion toxicity [36]. The results obtained in the present
applications of biochar, humic substances, and gypsum could mitigate part of these negative effects study indicate that
applications of biochar,
on quinoa plants.humic substances,
Agricultural and gypsum
productivity could mitigate
in saline–sodic soils part
can beof these negative
recovered effects
through theon
quinoa plants. Agricultural
application of combined productivity
amendments in saline–sodic soils can be
due to the restorative recovered
effect of these through
amendmentsthe application
on the
physical,
of combined chemical and
amendments biological
due conditions of
to the restorative theseofsoils,
effect these in amendments
this way the quinoa
on thecould be cultivated
physical, chemical
and biological conditions of these soils, in this way the quinoa could be cultivated in soilsBcharacterized
in soils characterized by excess salt problems. In fact, the combined application of + HS + G
by excessresulted in a significant
salt problems. increase
In fact, the in root biomass
combined in AZ-51 of
application genotype,
B + HSbut +G theresulted
highest increases were
in a significant
observed in AZ-103 genotype with the same treatment (Table 1). This may be explained because the
increase in root biomass in AZ-51 genotype, but the highest increases were observed in AZ-103
combination of HS and B induces exudation of organic compounds produced by the plant
genotype with the same treatment (Table 1). This may be explained because the combination of HS and
microbiota, which positively affects root development [37,38]. Additionally, the fact that B can
B induces exudation
exclude of organic
salts from compounds
root system can also produced
account byforthe
thisplant microbiota,
situation which positively
[39]. Combinations affects
of organic
root development
amendments[37,38]. Additionally,
and G significantly the factsoil
improved thatproperties,
B can excludewhich salts from
in turn root system
supported can
prolific also
root
accountgrowth
for thisofsituation [39]. Combinations of organic amendments and G
plants [40]. Similar results were also found by Kammann et al. [37], who observed significantly improved
soil properties,
enhancedwhich in turn(fine
root growth supported
root mass) prolific rootplants
in quinoa growth afterofBplants [40]. Similar
applications. Accordingresults were et
to Akhtar also
found by al.Kammann
[39], B positively affects
et al. [37], who plant root growth
observed underroot
enhanced saline conditions,
growth due to
(fine root its high
mass) adsorption
in quinoa plants
capacity, which
after B applications. might lead
According to to reduce
Akhtar et Na uptake
al.+[39], or enhanced
B positively Na+ plant
affects exclusion
root or both from
growth under roots.
saline
These observations are in agreement with the results obtained in this
conditions, due to its high adsorption capacity, which might lead to reduce Na uptake or enhanced study as significant
+ decreases
were obtained in leaf Na+ concentrations in amended soils (data not shown). Humic substances
Na+ exclusion or both from roots. These observations are in agreement with the results obtained in
improve soil microbial activity because of their auxin-like hormone activity, which stimulates root
this study as significant decreases were obtained in leaf Na+ concentrations in amended soils (data not
morphology [38].
shown). Humic substances
In terms of SPADimprove
chlorophyllsoil index,
microbial activity
the results because
show of their
significant auxin-like
increases in allhormone activity,
treated soils in
which stimulates root morphology [38].
AZ-103 genotype (Table 2). When submitted to saline conditions, chlorophyll content generally
In terms of SPAD chlorophyll index, the results show significant increases in all treated soils
in AZ-103 genotype (Table 2). When submitted to saline conditions, chlorophyll content generally
decreases in salt-sensitive plants, whereas it increases in salt-tolerant species [41]. This is consistent
with our results since the unamended treatment showed a significantly lower SPAD index value.
This indicates that amendments have a positive effect as their applications result in increased
chlorophyll content in plants under salinity stress. This is in agreement with Ramzani et al. [10],
who confirmed that chlorophyll content in quinoa plants grown under saline conditions was positively
affected by B and compost applications compared to the control treatment. Nevertheless, AZ-51
Sustainability 2018, 10, 3083 11 of 17
genotype showed no significant response in terms of SPAD values (Table 2). In fact, this might be related
to genetic diversity between genotypes, possibly due to leaf internal mechanisms in AZ-51 plants.
This may allow a better adaptation to salinity conditions, maintaining an adequate photosynthetic
activity. Based on this, responses were not so evident to amendment applications. Some genotypes
present salt adapting mechanisms with physiological responses that result in phenotypic plasticity of
leaves to abiotic stress. Therefore, leaf morphological traits, such as associated photosynthetic function,
vary depending on the environment and its genetic plasticity [42].
Most of amendment applications (individual and combined) tested in this study showed
statistically significant increases in stomatal conductance respect to untreated soil (Table 2).
These results agree with those reported by Akhtar el al. [43], who described that B incorporation
into the soil increased both stomatal aperture and density, which implies reduced stress in wheat
plants. This can be also attributed to B as it can enhance soil water-holding capacity, which should
help mitigate salt-induced osmotic stress and ion toxicity to plants due to dilution effect. Moreover,
HS increased photosynthesis and respiration rates in plants due to the presence of phytohormones,
such as auxin and gibberellins; these are directly involved in various biochemical mechanisms inside
plant cells and enzymatic activities involved in carbohydrate metabolism [44]. Conversely, stomatal
conductance decreased in unamended soils in this study due to stomatal closure. To endure osmotic
constraint, salt-tolerant plants are more restrictive with water loss via transpiration by a sensitive
stomatal closure mechanism; this leads to a restricted availability of CO2 for carboxylation reaction,
which favors the formation of Reactive Oxygen Species (ROS) [45].
Salt stress has also been identified as a major factor limiting crop productivity in saline–sodic
soils [36]. The results show that quinoa seed yield significantly increased in G; and HS + G (in AZ-51
genotype). Similarly, all treated soils in AZ-103 genotype improved seed yield significantly (Figure 1).
Similar results have been reported by Lashari et al. [46], who evaluated wheat growth in salt-stressed
soils and found increases in grain yields after B and compost applications. This could be attributed to
multiple effects by amendment applications on quinoa plants grown in salt-affected soil, such as root
development, hormonal and metabolic activity leading to higher seed yield. In fact, HS increased root
growth through indole acetic acid (IAA), resulting in enhanced root surface area, and thus enabling
plant access to nutrients and boosting yield [47]. In addition, Turan et al. [48] indicated that increases
in seed yield may be explained because HS increase the production of adenosine triphosphate (ATP)
within plant cells and thus increase permeability, resulting in rises of nutrient transport to sites of
metabolic demand. Another study reported that, B application supplied nutrients to plants, triggered
changes in soil redox conditions, enhanced microbial biomass, and increased water holding capacity,
increasing plant tolerance to saline stress and also plant dry yield [22]. Moreover, Spokas et al. [49]
suggested that B amendments incorporated into the soil are an ethylene source that stimulates plant
growth and yield, and Agegnehu et al. [50] conducted a study that evaluated the effects of B on soil
quality and maize growth. These authors indicated that B increased growth and grain yield due to
greater pore spaces, leading to a higher nutrient supply to plants. Likewise, Mahmood et al. [51],
reported significant improvement on wheat plant growth and yield (25% to 43%) in saline–sodic soils
reclaimed with G, which has been attributed to increases in Ca+2 build-up, elimination of Na+ toxicity
and nutritional balance in plants. Although G and HS improved productivity of AZ-51 genotype, B
did not significantly increased genotype yield, probably because the contribution of labile or leachable
C and some nutrient fractions were very transient [22], considering that this genotype exhibited a late
maturation compared to AZ-103 genotype (25 days after). The B and HS rate is another factor that
could have limited the effect on this variable [52], since this genotype had a higher average yield of
45% (greater export of nutrients) than the genotype with early maturation.
Polyphenol content was evaluated as a functional quality indicator of quinoa seeds whose role is
to reduce the damages caused by ROS (Table 3). Most of the treatments did not affect the GAE content
significantly. Both genotypes presented a certain degree of tolerance to the salinity level of the soil
under study. This could have a negative influence on the induction to protective mechanisms, such as
Sustainability 2018, 10, 3083 12 of 17
polyphenol synthesis. Quinoa plants might use enzymatic antioxidant and non-enzymatic antioxidant
compounds as polyphenols, which have a strong ability to scavenge ROS [53]. This was supported by
Ruiz et al. [6], who reported that seeds harvested from R49 and VR quinoa genotypes, grown in saline
soils, showed higher GAE content compared to control treatments.
The highest significant protein content was obtained in quinoa seeds grown in HS and B treatments
in AZ-51 and AZ-103 genotypes, respectively (Table 3). These findings agree with results of previous
experiments in which organic amendment applications into a saline soil improved the nutritional
quality in quinoa seeds [10]. A similar response was observed in wheat grains grown in calcareous
soils [54]. This increased protein content of quinoa seed could be explained by the role of organic
amendments for overall improvement in soil health and delivery of essential nutrients to plants [55].
In addition, reduction in salt toxicity to plants through the adsorption of Na+ on large B surface
areas in the soil might be another possible mechanism for the increase in protein content of quinoa
seeds [22,56].
Soil salinity also generates osmotic effects in plants and often causes physiological drought if it
exceeds a critical threshold in crops [57]. Amendment applications improved chemical properties of
soils (decreases soil salinity), influenced by effective salt leaching from soil profile. In our experiment,
most of amended soils (except B treatment in AZ-51 genotype) showed significant decreases in soil
ECe compared to control soils (Table 4), suggesting that these amendments have a strong efficiency
in reducing soil ECe. Similar results were also reported by Tejada et al. [16] and Gupta et al. [17],
who reported that soil EC was significantly lower when organic amendments and G were applied to
reclaim salt-affected soils compared to the control.
Application of chemical and organic amendments increases the concentration of Ca2+ and
promotes the displacement of adsorbed Na+ . We found that SAR and ESP values reduced significantly
in all amended soils. These results agree with a study of Chaganti et al. Ref. [58], who found that
organic amendments (biochar, biosolids, green waste compost) improved soil hydraulic conductivity,
thus facilitating salt leaching of saline–sodic soil and allowing for a significant decrease in soil ESP
and SAR. Moreover, Mahmoodabadi et al. [13] reported that organic amendments decreased soil SAR
due to a reduction in Na+ solution concentrations and enhanced Ca2+ supply. Relative changes in
soil exchangeable Na+ are dependent on chemical reactions in the soil matrix. Chemical reactions
take place between soil solution and exchange phases due to changes in chemical concentrations of
monovalent and divalent cations [23]. In this regard, Nan et al. [57] applied G and HS in a sodic
soil and observed improved structural stability and a reduction of ESP from soil colloids. In this
sense, salts could be leached down to deeper layers. Moreover, Vijayasatya et al. [23] reported
that B incorporation to saline–sodic soil reduced ESP by 83% when compared to the control after
leaching. Likewise, Aktar et al. [39,43] attributed the reduction of soil salinity with B to: (1) the
adsorption/retention of salts, such as Na+ on biochar surfaces, or salt physical entrapment in B fine
pores, and (2) biochar-induced reduction in upward movement of saline water.
Significantly higher concentrations of soil exchangeable cation (Ca2+ ) were observed after
the application of combined amendments and G treatments (Table 5). These results suggest that
HS, B, and G have a synergistic effect to carry more Ca2+ into the soil solution. HS, B, and G
increased Ca2+ content in saline–sodic soil, which improved exchange of sodium from soil exchange
sites [14,15,57,58]. Nevertheless, the individual application of (B) and (HS) did not significantly
increased soil exchangeable cation (Ca2+ ) or this increase was very low (e.g. HS in AZ-103 genotype;
Table 5). This could be probably attributed to the chemical composition of Biochar (0.8% Ca).
Some differences in the final concentrations of bivalent cations (e.g. Ca, Mg) arise from the
chemical composition of applied organic amendments [13]. In the present study, soil exchangeable
Mg2+ did not increase significantly after amendment applications (Table 5). These results agree with
the findings of Chaganti et al. [23], who applied composts and B in a saline–sodic soil and found that
exchangeable Mg2+ concentrations did not differ statistically respect to untreated soil.
Sustainability 2018, 10, 3083 13 of 17
It is widely acknowledged that divalent cation Ca2+ can replace adsorbed Na+ in soil colloids,
causing flocculation of colloids and improving soil structure [59]. This is a key point for a successful
reclamation of saline–sodic soil. We found that soil exchangeable Na+ concentrations significantly
decreased in all treated soils respect to untreated soils (Table 5). These results are in agreement with
previously reported findings [13,17,57,58]. Nevertheless, individual applications of B and HS did not
increase Ca2+ concentrations in soil but they significantly decreased Na+ concentrations; these effects
might be explained by HS and B applications to saline soils, resulting in reductions of sodium salt
concentrations, which is not correlated with salt leaching, yet it may be correlated with improving root
growth and accumulation of Na+ in the root surface area (biochar) [22,60].
Several processes and materials able to alter soil C content can affect biomass and activity of
microbial communities. B and HS can improve the growth of microorganisms in salt-affected soils
in many ways, including: increasing water retention and supply to microbes, releasing soil nutrients
for microbes, stimulating root exudation of dissolved organic carbon and nitrogen, which are needed
for microbial metabolism. We found that soil microbial biomass (FDA) significantly increased with
most of the treatments in both quinoa genotypes, except with the G treatment in AZ-51 genotype,
which was similar to the control (Figure 2). These results are consistent with our hypothesis that B and
HS enhance soil microbial activity. Zheng et al. [24] noticed that B (peanut Shell 350 ◦ C) induced a
microbial response in the rhizosphere. Moreover, Bhaduri et al. [61] also reported that B application
(peanut Shell 300 ◦ C, in 5% dose) on saline soil influenced microbial growth and C use efficiency led
to increases in soil microbial biomass. According to Pukalchik et al. [62], addition of HS stimulated
heterotrophic microorganisms in the soil, and consequently restored soil microbial respiration in
multi-contaminated soils. Our results indicate that there is a synergistic effect between B + HS + G
that leads to enhancements in soil microbial biomass and respiration (Figures 1 and 3). The positive
effect of B on microbial biomass can be explained because the internal pore system of B particles may
protect microorganisms. Microbial sorption to B may occur via flocculation, adsorption on surfaces,
and entrapment in a matrix [22]. According to Whitman et al. [63], microbial responses to B addition
could be attributed to modified substrate availability (e.g. C and N), due to labile C input from
biochar and soil chemical properties such as salt stress (e.g. ECe, ESP, Table 3). On the other hand,
microorganisms can be stimulated by a HS addition through enriched surfactant-like interaction.
Lipczynska-Kochani et al. [64] suggested that HS have direct effects on enzymes and oxidative stress
defense. In addition, HS should be considered as a significant carbon source for soil bacteria [64].
Control soils showed values of microbial biomass FDA (enzymatic activities) significantly lower than
those observed in other treated soils (Figure 3), which indicates that biochemical quality is negatively
affected by saline–sodic soils. This may be due to a salting-out effect, which involves a decrease in
enzyme solubility through dehydration (osmotic effect), thus altering enzyme catalytic sites [16,65].
Consequently, the application of combined amendments may be considered as a promising
technique to enhance the biological quality of saline–sodic soils. However, the role of biochar in soil
biological processes represents a frontier in soil science research, with many unexplained phenomena
that require further research [22].
5. Conclusions
The combination of biochar, humic substances and gypsum (B + HS + G) resulted in the highest
increases in root biomass in both AZ-51 and AZ-103 quinoa genotypes. Stomatal conductance,
SPAD index, and seed yield increased significantly in all treated soil as compared to the control
in AZ-103 genotype, while increases were also observed in the most of the treatments of AZ-51
genotype. Seed yield doubled in AZ-51 after applications of G; and HS + G; whereas similar increases
were obtained in all amended soils in AZ-103. Seed quality (protein content) was positively affected by
B and HS amendment applications. These results suggest that each genotype responded differentially
to amendment applications. On the other hand, soil sodicity and salinity (ESP; ECe) were significantly
reduced with all individual and combined amendments. The most effective treatments in reducing
Sustainability 2018, 10, 3083 14 of 17
sodicity levels through increases in soil exchangeable Ca2+ concentrations were: G; B + G; B + HS; and
B + HS + G. Moreover, soil microbial biomass was mostly stimulated with the B + HS + G combined
treatment. In this sense, the use of combined amendments improved the chemical and biological
properties of the soil, reducing the negative effects of saline–sodic soil on the growth of quinoa
genotypes. This paper provided the first results regarding the performance of AZ-51 and AZ-103
quinoa genotypes when grown in saline–sodic soil and their responses to different amendments.
Field trials are required to fully understand the behavior of the most effective treatments identified in
this experiment (B + HS + G; B + G; and B + HS).
Author Contributions: M.A. and M.S. (Mauricio Schoebitz) conceived designed and performed the experiments.
M.A., A.Z.-S., M.S. (Marco Sandoval), C.M., and M.S. (Mauricio Schoebitz) analyzed the data and contributed to
the writing of the paper. All authors read, discussed, and approved the final manuscript.
Acknowledgments: This research was supported by Fondecyt Initiation Project Nº 11170254.
Conflicts of Interest: The authors declare no conflict of interest.
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