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100
GUOHUA XU ET AL.
Table I
Chloride Concentrations in Some Natural Sourcesa
Source
Chloride (g/kg)
Earth crust
Lithosphere
Basalt rocks
Syenite
Igneous rocks
Shale
Sandstone
Limestone
Dolomite
Soils
Ocean
Plants
Low to medium saline water
High to very high saline water
Table salt (NaCl)
Potassium chloride (KCl)
1.50
0.48
0.50
0.98
0.23
0.16
0.02
0.37
0.50
0.10
19.0
1.0 –10.0
0.10 – 0.30b
0.30 –1.20b
607
450 –570
aCompiled
bUnit:
from Yaalon (1963) and Flowers (1988).
g/liter.
coast, many soils and crops receive a more than adequate supply of chloride from
wind-borne sprays of rain and snow (McWilliams and Sealy, 1987). The amount of
chloride derived from the atmosphere ranges from 17.6 to 36.0 kg/ha per year
(Reynolds et al., 1997). The salt concentration in the air decreases exponentially with
increasing distance from the shore, becoming uniform at about 50–150 km from the
shore. The salt concentration in the air depends on topography, wind direction, and
storm distribution (Yaalon, 1963). Cl concentrations of 20–50 mg/liter have been
found in rainwater close to the shore, diminishing rapidly with distance from the
ocean. In inner continental areas the corresponding concentrations are 2–6 mg/liter.
The quantity of Cl deposited annually is about 175 kg/ha near the sea, but only 50
kg/ha at a distance of 6 km from the sea (Yaalon, 1963). Midcontinental areas such
as the Great Plains of North America receive less than 1.0 kg Cl/ha annually through
precipitation (Junge, 1963). Atmospheric Cl inputs often increase near heavily industrialized areas where large quantities of coal are burned (Fixen, 1993).
3. Addition of Chloride via Irrigation and Fertilization
The amount of Cl added to a field via irrigation water and municipal effluents
depends on farm activities. Water of low to medium salinity contains 100–300 g
Cl/m3 (Table I), whereas saline water contains 300–1200 g Cl/m3.
It is estimated that by the year 2000, the total annual amount of Cl used in fer-
ADVANCES IN CHLORIDE NUTRITION
101
tilizers in China, mainly as NH4Cl and KCl, will be 5 ϫ 109 kg (Pan et al., 1991a;
Yin et al., 1989). For each hectare of soil, the amount of Cl introduced by 500 mm
of irrigation water containing only 200 g Cl/m3 is 1000 kg. This is four times more
than the amount of Cl applied by fertilization with KCl at 500 kg/ha.
B. CHLORIDE IN SOIL
The chloride anion is not adsorbed on soil particles at neutral and basic pH values and is therefore leached easily. In Cl-deficient soils, the optimal depth for soil
sampling to estimate Cl availability to plants depends on the rooting characteristics of the crop, as well as the cropping system, soil type, precipitation or frequency
of irrigation, and drainage. In paddy soil, a large amount of Cl was washed to a
depth of 40 –60 cm by water after one season of rice growing (Huang et al., 1995).
In the North American Great Plains, sampling down to 60 cm was recommended
for spring wheat and barley (Fixen et al., 1987).
1. Reaction of Chloride with Clay Surfaces
The assumption that chloride ions, such as nitrate and perchlorate ions, are
adsorbed onto positive sites on clay particles through electrostatic attraction (Borggaard, 1984) is the theoretical basis for determination of the positive surface charge
of soils, as suggested by Schofield (1949). The real behavior of Cl in variableϪ
charge soils differs, however, from that of NOϪ
3 or CIO4 (Wang and Yu, 1998).
The diffusion coefficient of Cl is smaller than that of NOϪ
3 . X-ray photoelectron
spectroscopic studies showed that Cl but not NOϪ
reacted
with
the soil surface ( Ji,
3
1997). The pH values of the suspensions in a HCl-treated system and a HNO3treated system differed in the variable-charge soil, but not in the permanent charge
soil (Table II). Therefore, at least for Cl at low pH in variable-charge soils, a specific adsorption mechanism is involved. As Cl concentration increases, Cl replaced
more OHϪ than H2O (Wang and Yu, 1998). The release of OHϪ ions during the
specific adsorption of chloride decreased on removal of the free iron oxides. This
hydroxyl ion release, caused by specific adsorption of Cl, increases the soil pH value in chloride solutions (Zhang et al., 1989).
2. Plant Uptake
Crop foliage can remove substantial amounts of Cl, especially when soil levels
of available Cl are high. At peak accumulation, the Cl content of spring wheat was
18 and 61 kg/ha on sites testing low and high in Cl, respectively (Schumacher,
1988, cited by Fixen, 1993). By the time of crop maturity, Cl in the portion of the
plant above ground had dropped to 50 and 43% of these values, respectively, meaning that it had returned to the soil. Similar behavior was reported for potassium in
102
GUOHUA XU ET AL.
Table II
Changes in pH of Soil Suspensions of a Rhodic Ferralsol and a Cambisol
after the Addition of Different Quantities of HCl or HNO3a
pH value
Rhodic Ferralsol
Cambisol
Acid added
(mmol/kg)
HCl
HNO3
HCl
HNO3
0
4
8
10
12
14
16
18
20
5.60
5.17
4.79
4.56
4.36
4.26
4.05
3.98
3.83
5.60
5.09
4.64
4.37
4.23
4.04
3.81
3.65
3.37
7.00
6.12
5.17
5.06
4.99
4.67
4.31
4.33
4.23
7.00
6.08
5.13
5.02
4.94
4.70
4.35
4.29
4.20
aBased
on Wang and Yu (1998).
wheat (Kafkafi et al., 1978). The removal of Cl in grains is very limited. In spring
wheat, soybean, and rice, the amount of Cl distributed in the grains was only 2.15,
1.34, and 1.62%, respectively, of the crop’s total Cl uptake (Pan et al., 1991b). The
concentration of Cl in dry matter wheat grain is only 0.05% (Knowles and Watkin,
1931). Removal of Cl in soybean seed amounts to 0.45 kg/ha, which is less than
the amount deposited annually in rainfall (Parker et al., 1986).
C. CHLORIDE AS A NITRIFICATION INHIBITOR
Ammonia fertilizers differ in their rates of nitrification (Meelu et al., 1990). Nitrification of 300 mg NH4Cl/kg in an acid soil (pH 5.6) at 30ЊC was only 6% after 21 days as compared to 75% in the case of urea (Hauck, 1984). However, differences in nitrification rates among N sources decreased markedly in alkaline soil
(pH 8.2), except when high N rates above 400 mg/kg were applied. Whereas all
N added as urea was nitrified in 10 days, it took 35 days for the nitrification of only
91% of 300 mg N/kg as ammonium chloride (Meelu et al,. 1990). While 80% of
ammonium sulfate was nitrified in 12–18 days, it took 30 –35 days for the nitrification of ammonium chloride to the same extent (Babriwara, 1959, cited by VedeNarayanan, 1990). The relative inhibition of ammonium chloride nitrification was
attributed to differences in osmotic potential under different saline conditions or
to a direct effect of Cl (Roseberg et al., 1986).
Results of field and laboratory studies indicate that nitrification in moderately
103
ADVANCES IN CHLORIDE NUTRITION
acid soils (pH 5.0–5.5) is reduced both by Cl and by low osmotic potential of the
soil solution (Christensen et al., 1986). In soils in which the osmotic potential was
increased four-fold by the addition of ammonium salts of chloride or sulfate, the
nitrification of applied NHϩ
4 was slowed both by Cl and by the decreasing osmotic potential of the N solution (Table III). Addition of a Ϫ93-kPa solution of Cl salt
to the soil resulted in a lower nitrification rate than that obtained with a Ϫ680-kPa
SO42Ϫ solution. The nitrification essentially stopped when a Cl salt solution of
Ϫ338 or Ϫ680 kPa was added. The chloride ion functions as a nitrification inhibitor in the soil at pH 5.5 but not at pH 6.6 (Christensen et al., 1986). In slightly acid soils (pH 6.5–7.0), however, the impact of the Cl ion on nitrification is
much lower. The slow rate of nitrification inhibition induced by chloride fertilization, particularly in slightly acid soils, might help to increase N use efficiency in
rice fields by preventing N losses due to denitrification in the event of flooding.
III. CHLORIDE IN PLANTS
A. YIELD AND QUALITY RESPONSE TO CHLORIDE
1. Positive Yield Response to Chloride
Chloride deficiencies in plants generally occur in inland soils (Fixen, 1987).
Substantial responses to Cl-containing fertilizers have been reported for different
Table III
Effects of Soil pH and Osmotic Potential of Added Ammonium Chloride and Ammonium
a
Sulfate Solutions (100 mg NH؉
4 -N/kg soil) on Nitrification Rate
Soil
Soil pH
Woodburn
5.3
5.3
5.3
5.3
Nekia silt
Clay loam
4.9
5.5
6.2
aBased
Osmotic potential of
added NHϩ
4 solution
(kPa)
Ϫ93
Ϫ171
Ϫ338
Ϫ680
LSD ( p ϭ 0.01)
Ϫ93
Ϫ93
Ϫ93
LSD ( p ϭ 0.01)
on Christensen et al. (1986).
Nitrification rate
(mgNOϪ
3 -N/kg и day)
NH4Cl
(NH4)2SO4
1.4
0.82
0.1
Ϫ0.07
2.4
2.12
1.88
1.75
0.24
5.8
11.2
13.8
8.8
13.2
14.4
0.48
104
GUOHUA XU ET AL.
crops in many parts of the world; e.g., coconut (von Uexkull and Sanders, 1986),
corn (Heckman, 1995), kiwifruit (Smith et al., 1987), oil palm (von Uexkull,
1990), potato (Gausman et al., 1958b), spring wheat and barley (Fixen et al., 1986;
Engel et al., 1994), tobacco (Li et al., 1994), and sugar beet (Zhou and Zhang,
1992). Typical symptoms of Cl deficiency include wilting of leaves, curling of
leaflets, bronzing and chlorosis similar to those seen with Mn deficiency, and severe inhibition of root growth (Ozanne et al., 1957; Smith et al,. 1987).
The concentration range of chloride deficiency in plants varies between 0.13 and
5.7 mg/g for spinach and sugar beet, respectively (Table IV). In wheat, the Cl concentration of leaf tissue at heading is a good predictor of the response to Cl fertilization (Engel et al,. 1998); the critical range is between 1.5 and 4 mg/g DM, above
which no further response is expected.
In pot experiments, positive responses to chloride at 100 –200 mg/kg soil were
reported for white potato, peanut, tomato, and young may trees and at 100 –1600
mg/kg soil for sugar beet (Jing et al., 1992). On a sandy loam soil, chloride applications of up to 400 kg/ha yielded 500 –1500 kg/ha more corn grain than was
obtained in the control (Heckman, 1995). Grain yields of corn were correlated positively with increases in Cl concentrations in the leaf ears. In wheat, there was no
yield response to Cl fertilization when the Cl content was above 70 kg/ha in the
top 12 cm of soil (Fixen et al., 1987). Yield increases due to Cl fertilization from
sources such as KCl, CaCl2, NH4Cl, and NaCl have also been associated with the
suppression of foliar or root diseases of wheat (Christensen et al., 1981; Engel et
al., 1997). Ammonium chloride produced yields of rice that were equal to or higher than those obtained with urea and ammonium sulfate. In a greenhouse study,
rice yields with ammonium chloride were significantly inferior to ammonium sulfate, especially at high salinity levels (Meelu et al,. 1990). Yields of sugarcane fertilized with ammonium chloride exceeded or equaled those of ammonium sulfate
at 67–225 kg N/ha (about 170 –570 kg Cl/ha) (Veda-Narayanan, 1990).
2. Crop Sensitivity or Tolerance to Chloride
Sensitivity to high Cl concentrations varies widely between plant species and
cultivars. Generally, most nonwoody crops tolerate excessive levels of Cl, whereas many woody plant species and beans are susceptible to Cl toxicity (Maas, 1986).
The critical toxicity concentration is about 4–7 and 15–50 mg/g for Cl-sensitive
and Cl-tolerant plant species, respectively (Table IV). For a ‘Washington’ navel
orange cultivar grafted on the poor chloride excluder rootstock ‘Rough Lemon,’
when the Cl of the leaf is higher than 2 mg/g the fruit yield declines linearly with
leaf Cl content (Fig. 1). However, mature leaves of citrus were able to tolerate Cl
concentrations of up to 350 mmol/liter in leaf tissue water or approximately 25
mg/g DM under glasshouse conditions without sustaining permanent damage to
the photosynthetic system (Walker et al., 1982).
Table IV
Chloride Concentrations in Plants
Concentration ranges of tissue Cl (mg/g DM)
Crop
Alfalfa
Apple
Avocado
Barley
Citrus
Coconut palm
Corn
Corn
Cotton
Grapevine
Kiwifruit
Lettuce
Pear
Peach
Peanut
Potato
Potato
Red clover
Rice
Rice
Soybean
Spinach
Spring wheat
Strawberry
Subterranean clover
Sugar beet
Sugar beet
Tobacco
Tomato
Wheat
aThe
Latin name
Plant part
Deficient
Normal
Toxicitya
References
Medicago sativa L.
Malus domestica
Persea americana Mill.
Hordeum vulgare L.
Citrus sp. L.
Cocos nucifera L.
Zea mays L.
Z. mays L.
Gossypium hirsutum L.
Vitis vinifera L. ssp. vinifera
Actinidia deliciosa
Lactuca sativa L.
Pyrus communis
Prunus persica
Arachis hypogaea L.
Solanum tuberosum L.
S. tuberosum L.
Trifolium pratense L.
Oryza sativa L.
O. sativa L.
Glycine max L. Merr.
Spinacia oleracea L.
Triticum aestivum L.
Fragaria vesca
Trifolium subterraneum L.
Beta vulgaris L.
B. vulgaris L.
Nicotiana tabacum L.
Lycopersicon esculentum Mill.
Triticum aestivum L.
Shoot
Leaves
Leaves
Heading shoot
Leaves
Leaves
Ear leaves
Shoots
Leaves
Petioles
Leaves
Leaves
Leaves
Leaves
Shoot
Mature shoot
Petioles
Shoot
Shoot
Mature straw
Leaves
Shoot
Heading shoot
Shoot
Shoot
Leaves
Petioles
Leaves
Shoot
Heading shoot
0.65
0.1
0.9–2.7
6.1
Ͼ2.1
ϳ7.0
Ozanne et al. (1957); Eaton (1966)
Eaton (1966)
Bar et al. (1997); Lahav et al. (1992)
Engel et al. (1994, 1997)
Bell et al. (1997); Bar et al. (1997)
von Uexkull and Sanders (1986)
Parker et al. (1985)
Johnson et al. (1957)
Tan and Shen (1993)
Downton (1985); Eaton (1966)
Smith et al. (1987); Prasad et al. (1993)
Johnson et al. (1957); Wei et al. (1989)
Robinson (1986)
Robinson (1986); Eaton (1966)
Wang et al. (1989)
Corbett and Gausman (1960)
James et al. (1970); Bernstein et al. (1951)
Whitehead (1985)
Yin et al. (1989)
Huang et al. (1995); Zhu and Yu (1991)
Parker et al. (1986); Yang and Blanchar (1993)
Robinson and Downton (1984)
Fixen et al. (1986) Wang et al. (1989)
Wang et al. (1989); Robinson (1986)
Ozanne et al. (1957)
Ulrich and Ohki (1956); Terry (1977)
Ulrich and Ohki (1956) Zhou and Zhang (1992)
Li et al. (1994); Eaton (1966)
Broyer et al. (1954); Kafkafi et al. (1982)
Engel et al. (1994, 1997)
plant yields decline or the plant shows visible scorching symptoms in leaves.
1.2–4.0
2.5–4.5
ϳ1.5–4.0
Ͼ4.0
ϳ2.0
Ͼ6.0–7.0
1.1–10.0
ϳ4.0–7.0
10.0–25.0
0.7–8.0
6.0–13.0
2.8–19.8
Ͻ0.50
0.9–3.9
Ͻ3.9
2.0–3.3
18.0
Ͼ25.0–33.1
10.0–11.0
Ͼ15.0
Ͼ23.0
Ͼ10.0
10.0 –16.0
Ͼ4.6
12.2
44.8
5.1–10.0
0.3–1.5
Ͼ7.0–8.0
Ͼ13.6
16.7–24.3
3.7–4.7
1.0–5.0
Ͼ7.0
Ͼ5.3
Ͼ7.1–7.2
1.2–10.0
Ͼ50.8
Ͼ10.0
ϳ30.0
Ͼ32.7
0.05– 0.11
2.1
>0.14
Ͻ1.0
0.71–1.42
0.15–0.21
Ͻ3.0
Ͼ0.13
1.5
Ͼ1.0
0.71–1.78
Ͻ5.7
0.25
1.2–4.0
Ͼ4.0
106
GUOHUA XU ET AL.
Figure 1 Relationship between citrus fruit yield and leaf chloride content. Recalculated from Cole
(1985).
The tolerance order of common agricultural crops to chloride (Table V) is very
similar to the order of critical electrical conductivity (EC) values of saturated soil
extracts. This is to be expected given the relationship between the chloride salt
content and the ECs of salt solutions (Richards, 1954). The crop with the greatest
tolerance to chloride is sugar beet, which may contain up to 50.8 mg Cl/g in the
leaves (Zhou and Zhang, 1992). Chinese cabbage is sensitive to Cl; when the Cl
level in irrigation water reached 80 mg/liter, its dry matter percentage was decreased significantly (Yin et al., 1989). Corn is tolerant to high levels of soil Cl,
but soybean is sensitive (Parker et al., 1983, 1985). At soil chloride levels of 100–
200 mg/kg, even sensitive crops such as sweet potato, white potato, sugarcane,
and tobacco showed no negative effects in yield or quality ( Jing et al., 1992). The
critical tolerance values of rice and wheat to chloride were found to be 780–800
and 1000–1350 mg/kg in a clay soil, respectively, and 380–400 and 600–650 mg/
kg in a loam soil, respectively (Zhu and Yu, 1991). Because the water-holding capacity in clay soil is much higher than in loam soil, the critical Cl concentration in
saturated soil solutions is expected to be similar for the same crop in different soils.
The tolerance of a crop to Cl is not related directly to its concentration in plant
Table V
Critical Toxicity Concentrations of Chloride and ECe Values in Soil and in Saturated Soil Extracts, Listed in Order
of Increasing Tolerance to Chloride
Critical toxicity concentration
Crop
Strawberry
Bean
Onion
Carrot
Radish
Lettuce
Turnip
Pepper
Apple
Sweet potato
Grape
Corn
Flax
Potato
a,b,c
Critical toxicity concentration
mmol Cl/litera
ECe (dS/m)b
mgCl/kg soilc
10
10
10
10
10
10
10
15
1.0
1.0
1.2
1.0
1.2
1.3
0.9
1.5
1.7
1.5
1.8
1.7
1.7
1.7
250
15
15
15
15
100
250
300
400
800
500
500
Crop
Broadbean
Sugarcane
Cabbage
Spinach
Cucumber
Tomato
Broccoli
Sugar beet
Cowpea
Wheat
Sorghum
Sugar beet
Cotton
Barley
mmol Cl/liter
ECe (dS/m)
15
15
15
20
25
25
25
40
50
60
70
70
75
80
1.5
1.7
1.8
2.0
2.5
2.5
2.8
4.0
1.3
Selected and recompiled from Maas (1986), Ayers and Wescott (1985), and Jing et al. (1992), respectively.
Maximum Cl concentration in saturated soil extracts without loss in yield.
b
Maximum ECe value in saturated soil extracts without loss in yield.
c
Maximum soil Cl concentration above which yield decline to 95% of the maximum yield is observed.
d
From Tan and Shen (1993).
a
6.8
7.0
7.7
mgCl/kg soil
500
600
600
3200
600
700
1600
1600d
108
GUOHUA XU ET AL.
tissues as is shown for different varieties of grapevine (Fig. 2). Scions on ‘Dogridge’ rootstock contained the highest leaf chloride concentration but exhibited the
greatest growth and were the least affected by salinity. There was no relationship
between the amount of chloride in plant parts and cane weight. Similar findings
were reported by Skene and Barlass (1988) for two rootstocks of grapevine. Dry
matter yields of the whole plant and chloride levels in leaves of the salt-tolerant
avocado cultivar Degania-113 were higher than in the salt-sensitive cultivar Smith
(Bar et al., 1997). The salt-tolerant alfalfa variety accumulated considerably higher concentrations of Na and Cl than the salt-sensitive variety (Ashraf and O’Leary,
1994). The salt-tolerant and salt-sensitive accessions of safflower did not differ in
tissues Cl, Kϩ, or Ca2ϩ (Ashraf and Fatima, 1995). It seems likely that factors associated with vigorous growth or Cl compartmentation within the cell could offset the inhibitory effects of chloride accumulation. The level of accumulated Cl in
the plant should therefore not be considered the sole criterion of crop tolerance to
chloride.
Plants are generally more tolerant to soil salinity during cooler seasons than in
Figure 2 Effects of chloride in irrigation water on leaf lamina Cl content and cane dry matter of
Sultana grapevine scion grafted on three rootstocks. Recalculated and redrawn from Downton (1985).
ADVANCES IN CHLORIDE NUTRITION
109
warmer ones (Pasternak and De-Malach, 1995). The salt tolerance of citrus rootstock varies with the stage of seedling development (Zekri, 1993). Cucumber is
more salt tolerant during germination than during vegetative or fruiting stages
(Chartzoulakis, 1991).
Chloride toxicity in plants is often hard to diagnose, for two reasons: (1) it is
difficult to separate the effects of chloride from those of any accompanying cation,
commonly sodium; and (2) it is difficult to distinguish between the specific toxic
effects of ions and the cellular dehydration caused by their excessive external concentrations. Visual symptoms of marginal leaf necrosis due to chloride accumulation such as those seen in avocado (Fig. 3) (see also color insert) might be misleading, as similar symptoms in mango (Fig. 4) (see also color insert) are a result
of iron deficiency (U. Kafkafi, unpublished data). Citrus-sensitive plants shed their
leaves when exposed to salts but do not exhibit leaf necrosis (Bar et al., 1997).
3. Yield Quality and Chloride Content in Harvested Plant Parts
Salinity improves both fruit taste and appearance quality of tomato and melon
(Mizrahi, 1982; Mizrahi and Pasternak, 1985; Faiz et al., 1994). This phenomenon was attributed to the significantly higher content of total soluble solids and
of aromatic and other components found in these fruits under saline condition
(Davies and Hobson, 1981). Most of the reported salinity effects are to the integrated
Figure 3 Relieving chloride toxicity in avocado leaves by increasing nitrate concentration in irrigation water containing 16 mM Cl (Y. Bar, M.Sc. 1986 Rehovot, Israel) (see also color insert).
110
GUOHUA XU ET AL.
Figure 4 Marginal leaf necrosis symptoms in mango due to iron deficiency. Visual symptoms are
similar to chloride toxicity (U. Kafkafi, unpublished results) (see also color insert).
action of both Na and Cl. The specific influences of chloride on the quality of agricultural products are not clear. Wang et al. (1989) found that the soluble sugar and
vitamin C contents in the fruit of strawberry grown in soil containing Cl at 100–200
mg/kg soil were significantly higher than in soil containing 37 mg Cl/kg soil.