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NUTRIENT REQUIREMENTS OF CHAMAEROPS HUMILIS L. AND

WASHINGTONIA ROBUSTA H. WENDL PALM TREES AND THEIR
LONG-TERM NUTRITIONAL RESPONSES TO SALI....

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NUTRIENT REQUIREMENTS OF
CHAMAEROPS HUMILIS L. AND
WASHINGTONIA ROBUSTA H. WENDL
PALM TREES AND THEIR LONG-TERM
NUTRITIONAL RESPONSES TO SALINITY
a b
María Dolores Simón , Manuel Nieves-Cordones , María Jesús
c c a
Sánchez-Blanco , Trinitario Ferrández & Manuel Nieves
a
EPSO, Universidad Miguel Hernández , Alicante , Spain
b
Departamento de Nutrición Vegetal , CEBAS-CSIC , Murcia , Spain
c
Departamento de Riego , CEBAS-CSIC , Murcia , Spain
Published online: 18 Jun 2013.

To cite this article: María Dolores Simón , Manuel Nieves-Cordones , María Jesús Sánchez-Blanco ,
Trinitario Ferrández & Manuel Nieves (2013): NUTRIENT REQUIREMENTS OF CHAMAEROPS HUMILIS L.
AND WASHINGTONIA ROBUSTA H. WENDL PALM TREES AND THEIR LONG-TERM NUTRITIONAL RESPONSES
TO SALINITY, Journal of Plant Nutrition, 36:9, 1466-1478

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 Journal of Plant Nutrition, 36:1466–1478, 2013
Copyright ! C Taylor & Francis Group, LLC

ISSN: 0190-4167 print / 1532-4087 online

DOI: 10.1080/01904167.2013.794240

NUTRIENT REQUIREMENTS OF CHAMAEROPS HUMILIS L. AND

WASHINGTONIA ROBUSTA H. WENDL PALM TREES AND THEIR
LONG-TERM NUTRITIONAL RESPONSES TO SALINITY

Marı́a Dolores Simón,1 Manuel Nieves-Cordones,2 Marı́a Jesús

Sánchez-Blanco,3 Trinitario Ferrández,3 and Manuel Nieves1
1
EPSO, Universidad Miguel Hernández, Alicante, Spain
2
Departamento de Nutrición Vegetal, CEBAS-CSIC, Murcia, Spain
3
Departamento de Riego, CEBAS-CSIC, Murcia, Spain
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! The ornamental value of plants used in semiarid areas can be improved by knowledge of their
required nutrients and of their nutritional responses under saline conditions. We present a long-term
study concerning the nutritional status in Chamaerops humilis and Washingtonia robusta.
Two-year-old plants were grown for two years outdoors in pots using water with electrical conduc-
tivity values of 2 (control) or 8 dS m −1 (saline conditions). Nutrient specific absorption rates and
leaf nutrient transport rates were estimated by fitting a Richards function regression. We suggest
fertilizing C. humilis and W. robusta plants with nitrogen (N): phosphorus pentoxide (P2 O5 ):
dipotassium oxide (K2 O) ratios of 4:1:5 and 5:1:3, respectively. Diagnosis and Recommendation
Integrated System (DRIS) and Plant Analysis with Standardized Scores (PASS) norms were also
evaluated. PASS norms provided better nutritional diagnosis than DRIS norms. In saline condi-
tions, PASS-INI (Independent nutrient index) pointed to a deficiency (<−10) of phosphorus in
C. humilis and of nitrogen in W. robusta.

Keywords: palm tree, DRIS, PASS, salinity, biomass allocation, fertilizer recommenda-
tion.

INTRODUCTION
About 50% of irrigated land in the world is affected by salinity (FAO,
2008). Salinity may cause nutrient deficiencies or imbalances, due to the
competition of sodium (Na+) and chloride (Cl−) with nutrients such as
potassium (K +), calcium (Ca2+), and nitrate (NO3 −). Generally, these ion
interactions reduce the specific nutrient absorption rate (SAR) (Cramer

Received 14 November 2010; accepted 1 February 2012.

Address correspondence to Manuel Nieves, EPSO (Universidad Miguel Hernández), Ctra. Beniel
km 3.2, 03312 Orihuela, Alicante, Spain. E-mail: m.nieves@umh.es

1466
 Nutrient Requirements under Long-Term Salt Stress 1467

et al., 1991; Ruiz et al., 1997). Nutrient disturbances under salinity reduce
plant growth by affecting the availability, transport and partitioning of nu-
trients (Hu and Schmidhalter, 2005).
The accumulation of Na and Cl ions in leaves or changes in plant mor-
phology are, in general, long-term process in salt-stressed plants (Munns
and Tester, 2008). Although some studies exist on nutrition (Broschat and
Meerow, 2000) and the fertilizer requirements (Broschat, 1995, 1999) of
palm trees, there are few experiments documenting the long-term effects of
salinity on mineral nutrient absorption and transport to leaves and, conse-
quently, the response of these plants to such stress.
Young palm trees are regularly grown in nurseries for four years be-
fore being used for gardening or landscaping in arid and semi-arid regions
(Del Cañizo, 2002). Under these conditions, treated sewage water or aquifer
water, frequently with high levels of salinity, are used to irrigate many mu-
nicipal parks and golf courses, which may affect plant quality. It is therefore
important to use salt tolerant ornamental species in landscaping projects,
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xeriscape and public areas (Morales et al., 1998).

A study on salt tolerance in young palm trees (Simón et al., 2010) pointed
to higher biomass yields in Washingtonia robusta at salinity levels below elec-
trical conductivity (EC)water = 6 dS m−1, while Chamaerops humilis was more
tolerant to higher salinity levels. However, the causes of this higher tolerance
in C. humilis are not well known, although a nutritional effect is probably
behind the changes in salt tolerance. Adverse conditions frequently alter
the nutrient balance and impair yields, complicating leaf analysis interpre-
tation (Parida and Das, 2005; Hu and Schmidhalter, 2005). However, plant
analysis is an important tool for diagnosing and correcting plant nutrient
deficiencies and imbalances. Thus, adapted fertilizer management in W. ro-
busta and in C. humilis could attenuate salt effects (Hu and Schmidhalter,
2005).
Conventionally, leaf analysis has provided a guide for fertilizer applica-
tions, according to the sufficiency range (SR), a method based on construct-
ing independent nutrient indices, and including only one nutrient in each
index (Walsh, 1973; Jones et al., 1991). A second method is based on depen-
dent nutrient indices, in which each index includes two or more nutrients.
Diagnosis and Recommendation Integrated System (DRIS) is the princi-
pal example of this approach (Beaufils, 1973). One proposed variation of
DRIS is the incorporation of dry matter indices (Idm ) into what has been la-
beled Modified-DRIS (M-DRIS) (Walworth et al., 1986; Hallmark et al., 1987;
Hallmark and Beverly, 1991). Later, a mixed system was developed, Plant
Analysis with Standardized Scores (PASS) (Baldock and Schulte, 1996),
which has two sections: one based on an independent nutrient index (INI)
approach, as in the SR system, and the other based on a dependent nutri-
ent index (DNI) approach, as in the DRIS. In addition, there is an overall
index, the PASS yield index (PASS YI), which shows a better relationship
 1468 M. D. Simón et al.

between yield and nutrient deficiencies than the DRIS balance index (DRIS
BI) (Baldock and Schulte, 1996; Urricariet et al., 2004).
Knowledge of the nutrient amounts required by Chamaerops humilis and
Washingtonia robusta for optimum growth and of the nutritional response of
these palm trees to salinity can improve fertilizer management, their pro-
ductivity and ornamental value. This study was carried out to assess SR, PASS
and DRIS norms under saline conditions and whether these approaches are
complementary or one is better than the others.

MATERIALS AND METHODS

Plant Material and Growth Conditions
Two-year-old Mediterranean Fan palm (Chamaerops humilis L.) and Mex-
ican Fan palm (Washingtonia robusta) seedlings (56 plants of each) were
transplanted from a nursery (Elche, Spain) to 10 L pots (one plant per pot)
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containing a 60:40 (v/v) mix of brown:black peat moss. An equal number of

each type of plant was put in four uncovered ponds for irrigation delivered
from below, the water being absorbed upwards and the excess collected for
recycling. Plants were watered to saturation each week and fertilized every
second week with 0.5 g per plant of nitrogen (N)-phosphorus (P)- potassium
(K) complex [10-20-5 (w/w/w); Agrosuperior, Cartago, Costa Rica, 0.5 g per
plant of ammonium nitrate (NH4 NO3 ; 33.5% N), and 0.25 g per plant of
ethylenediamine (O-Hydroxy-P- Methylphenylacetic) acid (EDDhmA)- iron
[Fe; 3% (w/w) Fe]. All plants were sprayed to control pests as needed.

Experimental Procedure
Plants were grown for two years, outdoors (Elche, Spain), using sub-
irrigation water with electrical conductivities of (ECw) 2 (control) or 8 dS
m-1 (salt treatment). The characteristics of the irrigation water and climatic
conditions were described by Simón et al. (2010). After 1, 97, 218, 403, 510,
651, and 725 d, four plants of each species from each treatment were chosen
at random and harvested destructively. Plants were separated into leaves,
stems and roots and were rinsed in deionized water, blotted dry with paper
towels. The plant material was weighed after drying at 65◦ C for 48 h.

Plant Mineral Analysis

Plant samples were extracted with deionized water, and the tissue
chloride concentration was measured with a Corning 926 chloridometer
(Sherwood, UK). Tissue N concentration was measured using a Thermo-
Finnigan 1112 EA elemental analyzer (Thermo-Finnigan, Milan, Italy). Tis-
sue Na+, K +, magnesium (Mg2+), calcium (Ca2+), and P concentrations
 Nutrient Requirements under Long-Term Salt Stress 1469

were determined by inductively coupled plasma emission optical spectrome-

try (Iris Intrepid II, Thermo Electron Corporation, Franklin, MA, USA) after
acid digestion in nitric acid (HNO3 ): hydrogen peroxide (H2 O2 ) (5:3, v/v)
in a microwave reaching 200◦ C in 20 min and holding at this temperature
for 2 h (Mars Xpress, CEM Corporation, Matthews, NC, USA).

Nutritional Parameters
In control conditions, the amounts of each plant nutrient at the begin-
ning (1 d) and at the end (725 d) of the experiment were used to determine
total N-P-K uptake and the recommended of units of fertilizer (N-P2 O5 -
K2 O). The average efficiency of fertilizers used in the province of Alicante
can range from 55 to 75% (Legaz et al., 1993).
Leaf nutrient analysis from control plants harvested after 651 and
725 days was used to obtain the reference values for the nutrient sufficiency
range (SR), Diagnosis and Recommendation Integrated System (DRIS) and
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Plant Analysis with Standardized Scores (PASS). For the DRIS index, the
mean nutrient ratios presented were selected from each pair of inversely
related ratios (P: K, K: P) showing the lowest standard deviation (SD).
Tissue analyses were interpreted according to DRIS (Sumner, 1977),
M-DRIS (Walworth et al., 1986) and PASS (Baldock and Schulte, 1996).
For M-DRIS only elements with index values more negative than dry matter
index (Idm ) were considered potentially limiting. A highly negative Idm is
observed when samples are collected earlier than the stage of development
when tissue is usually sampled, so that element concentrations would be
higher than in the reference population. Thus, we used only the samples
from the last two harvests to calculate the indices (651 d and 725 d). PASS-
INI values between −10 to +10 are considered sufficient. Beyond that range,
a negative value was used to indicate nutrient deficiency and a positive value
indicated nutrient excess. The minimum value for the M-DRIS BI or PASS YI
is zero, so the closer these indices were to zero, the closer the nutrients were
to their optimum and the greater the yield potential. Conversely, the larger
the indices, the more distant the nutrients were from their critical level and
the lower the yield potential.

Leaf Nutrient Transport Rate and Specific Absorption Rate

Leaf nutrient transport rates, JL (mg g−1 day−1) are the rates of increase
in leaf nutrient contents over time, on a root dry weight basis (Pitman, 1988).

JL = (1/w R )(dN /dT )

The time trends in leaf nutrient contents (N ) and root dry weight
(w R ) were estimated by fitting a Richards function regression, wR (T ) = A
 1470 M. D. Simón et al.

TABLE 1 Total biomass (g), organ biomass (g) and biomass distribution among plant parts (%) in
Chamaerops humilis and Washingtonia robusta watered with 2 dS m−1 (Control) and 8 dS m−1 (saline)
during 725 days

Chamaerops humilis Washingtonia robusta

Total biomass Root Stem Leaf Total biomass Root Stem Leaf

Control 43.1 17.9 8.3 16.9 159.4 24.0 81.2 54.2

Saline 26.7 11.7 4.8 10.2 83.4 16.9 36.7 29.8
ANOVA ∗∗∗ ∗∗∗ ∗∗∗ ∗∗∗ ∗∗∗ ∗∗∗ ∗∗∗ ∗∗∗

Biomass allocation Biomass allocation

Control 41.5 19.3 39.2 15.1 50.9 34.0
Saline 43.8 17.9 38.2 20.3 44.0 35.7
ANOVA ns ns ns ∗∗∗ ∗∗∗ ns

Values are average from four replicates per seven harvesting dates (n = 28).Significant effects are
indicated by asterisks: ∗∗∗ , P = 0.001; ns indicates not significant at P = 0.05.
Downloaded by [Inra] at 07:45 19 June 2013

(1 + exp (b – k T ))ˆ(−1/v), where wR and T represent a series of paired

measurements of root dry weight and time, respectively (Causton and Venus,
1981). Then, ln-transformed dry weight was derived with respect to time, to
estimate the instantaneous JL values. The mean JL is calculated by dividing
the integral of instantaneous values, estimated as the sum of the daily values,
by the interval time.
The specific absorption rates, SAR (mg g−1 day−1) are the rate of in-
crease in plant nutrient contents over time, on a root dry weight basis. The
mean SAR values were calculated by the same method as used for mean JL
values.

Statistical Analysis
There were four replicates for each treatment, per genotype, and per
harvest date (i.e., 4 × 2 × 7). Differences in measurements between con-
trol and salt treatment were tested at the P ≤ 0.05 confidence level ac-
cording to Tukey’s test. All measured parameters were analyzed statistically
using SPSS Version 10.0 software (SPSS Statistical Package, Chicago, IL,
USA).

RESULTS
Biomass
Relative to the control, excess salt in the irrigation water induced a
lower reduction in vegetative growth in C. humilis (38.1% reduction) than
in W. robusta (47.7% reduction) (Table 1). Salinity did not change biomass
allocation in C. humilis, but in W. robusta the root mass fraction increased
(by 5.3%) and the stem mass fraction decreased (by 6.9%).
 Nutrient Requirements under Long-Term Salt Stress 1471

TABLE 2 Cl− and Na+ specific absorption rates (SAR), leaf transport rates (JL ) obtained by fitting a
Richards function regression (n = 28) and leaf ion concentrations and the indices of the ions (n = 8)
in saline treatment (S) relative to control (C) obtained from Plant Analysis with Standardized Score
(PASS; INI, Independent nutrient index; DNI, Dependent nutrient index) and modified
Recommendation Integrated System (M-DRIS; IN I, DRIS index)

SAR (mg kg−1 Leaf ion ξ (mmol M-

day−1) JL (mg kg−1 day−1) kg−1) PASS DRIS

C S C S C S INI DNI IN I

Chamaerops humilis
Cl− 3.21 4.71 0.66 1.03 263 315∗∗∗ 28 10 14
Na+ 1.96 2.68 0.16 0.26 37 60∗∗∗ 99 57 40
Washingtonia robusta
Cl− 6.65 5.47 1.64 1.36 399 407ns 7 −10 0
Na+ 2.89 2.33 0.65 0.37 95 96ns 10 6 −1

ξ Values are average from four replicates per seven harvesting date (n = 28).
Significant effects are indicated by asterisks: ∗∗∗ , P = 0.001; ns indicates not significant at P = 0.05.
Downloaded by [Inra] at 07:45 19 June 2013

Cl− and Na+

Cl− and Na+ specific absorption rates (SAR), leaf transport rates (JL ),
leaf ion concentrations and diagnostic indices (PASS and Modified-DRIS)
are given in Table 2. In C. humilis, salt treatment increased both SAR and JL.
Leaf ion concentrations increased significantly and PASS-INI showed very
high values for both ions. PASS-DNI and M-DRIS appointed to an imbalance
in both Cl− and Na+ with respect to the other nutrients. In contrast, in W.
robusta both SAR and JL were reduced when the Cl− and Na+ concentra-
tions in the irrigation water increased. Leaf ion concentrations did not show
significant changes as a result of salinity. The PASS INI showed values in a
range that indicated sufficiency (|INI| ≤ 10), and PASS DNI and M-DRIS
indices indicated a balance of ions (|Indices| ≤ 10).

Leaf Macronutrients
N, P, K, Ca and Mg specific absorption rates, leaf transport rates, leaf
nutrient concentrations and diagnostic indices (PASS and Modified-DRIS)
are shown in Table 3. In C. humilis, salt treatment decreased N, P and K SAR
by about 20%, and increased the Mg SAR by a similar percentage. Salinity
reduced the P JL by about 20% with respect to control JL , and increased N,
Ca and Mg JL . Leaf nutrient concentrations showed a significant decrease
in P levels and an increase in Mg levels. The PASS INI placed the nutrients
P (−16) and Mg (+31) out of the range from −10 to +10. The moderate
values of dry matter index (Idm) of −10 in C. humilis and −5 in W. robusta
suggested that harvested leaf samples were not so young. Only elements with
M-DRIS values more negative than Idm were considered potentially limiting.
The PASS DNI and M-DRIS indicated an imbalance with low values for N, P
 1472 M. D. Simón et al.

TABLE 3 N, P, K, Ca and Mg specific absorption rates (SAR), leaf transport rate (JL ), obtained by
fitting a Richards function regression, and leaf nutrient concentrations and the indices of the nutrient
in saline treatment (S) relative to control (C) obtained from Plant Analysis with Standardized Score
(PASS; INI, Independent nutrient index; DNI, Dependent nutrient index; Yi, yield index) and modified
Recommendation Integrated System (M-DRIS; IN I, DRIS index; Idm, dry matter index; BI, balance
index)

SAR (mg kg−1 JL (mg kg−1 Leaf ion ξ (mmol

day−1) day−1) kg−1) PASS M-DRIS

C S C S C S INI DNI YI IN I BI

Chamaerops humilis
N 6.28 5.08 2.84 3.18 1139 1066ns 0 −24 −14
P 0.47 0.38 0.20 0.16 64 49∗∗ −16 −24 −28
K 2.33 1.89 0.94 0.91 321 295 ns −8 −21 −16
Ca 1.52 1.60 0.40 0.68 214 213 ns 3 −13 0
Mg 0.96 1.18 0.32 0.47 115 145∗∗ 31 15 14
Idm −10
Overall
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Index 68 136
Washingtonia robusta
N 15.84 9.94 10.08 6.61 1232 1160 ns −13 −13 −11
P 0.65 0.64 0.24 0.21 62 70∗ 36 23 14
K 4.19 2.43 1.08 0.97 386 371 ns 0 −7 −8
Ca 7.02 4.13 2.25 1.55 347 367 ns 26 1 5
Mg 3.28 2.76 1.08 0.91 159 183∗∗ 50 −1 5
Idm −5
Overall 16 48
index

ξ Values are average from four replicates per seven harvesting date (n = 28).
Significant effects are indicated by asterisks: ∗∗∗ , P = 0.001; ns indicates not significant at P = 0.05.

and K, and high values for Mg. The overall indices showed high values, YI =
68 and BI = 136.
In control conditions, W. robusta showed higher SAR and JL values than
C. humilis for all nutrients. The salinity reduced the N, K and Ca SAR by
about 40%. However, salinity only produced slight reductions in P and Mg
SAR. Both nutrients exhibited significantly high leaf concentrations. The
PASS INI showed low values for N and high for P, Ca and Mg. The PASS DNI
and M-DRIS pointed to an imbalance, with low values for N and high for P.
The overall indices showed low values, YI = 16 and BI = 48.

N, P and K Uptake
The values of N-P-K nutrient uptake and the related fertilizer units of
Chamaerops humilis and Washingtonia robusta seedlings over the two years of
the experiment are shown in Table 4. C. humilis needed 77.7:4.1:28.7 mmol
per plant of N-P-K, respectively, over two years. The corresponding fertil-
izer units were 1.08:0.29:1.35 g per plant of N-P2 O5 -K2 O, respectively, with a
 Nutrient Requirements under Long-Term Salt Stress 1473

TABLE 4 Total N-P-K uptake per plant watered with 2 dS m−1 (Control) and 8 dS m−1 (saline) during
725 days, and the fertilizer recommendations for Chamaerops humilis and Washingtonia robusta seedlings

Absorption-based
Fertilizer units fertilizer
N-P-K Nutrients uptake recommendations(N-
uptake (N-P2 O5 -K2 O) N:P2 O5 :K2 O P2 O5 -K2 O)
Species Treatment (mmol/plant) (g/plant) Ratio (g/g) (g/plant)

C. humilis Control 77.7:4.1:28.7 1.09:0.29:1.35 4:1:5 2.0:0.5:2.5

Saline 22.7:2.6:14.4 0.32:0.18:0.68 2:1:4
W. robusta Control 334.6:13.8:58.4 4.68:0.98:2.75 5:1:3 8.5:2.0:5.0
Saline 122.5:11.1:20.8 1.72:0.78:0.98 2:1:1

balance in fertilizer units of 4:1:5. Consequently, for a fertilizer efficiency of

55%, it is necessary to apply 2.0:0.5:2.5 g per plant of N-P2 O5 -K2 O, respec-
tively. W. robusta required a higher nutrient dose for its growth. Thus, this
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species absorbed 334.6:13.8:58.4 mmol per plant of N-P-K, respectively over

two years. W. robusta showed a fertilizer balance of 5:1:3. Absorption-based
fertilizer recommendations were 8.5:2.0:5.0 g per plant of N-P2 O5 -K2 O, re-
spectively. However, about 70% of these amounts were taken up by the plant
during the second year of experiment (data not shown). In saline condi-
tions, plant macronutrient uptake was lower than in control conditions and
with different proportions of fertilizer units.

DISCUSSION
C. humulis and W. robusta exhibited different responses in growth, plant
morphology, ion uptake and leaf mineral composition under saline con-
ditions. W. robusta showed morphological plasticity in the face of salinity,
unlike that C. humilis. Both species showed similar biomass percentages in
leaves, whereas this parameter was higher in the roots of C. humilis than in
those of W. robusta (Table 1, 41.5 vs 15.1%), which may improve water and
nutrient absorption under drought stress conditions. However unless a plant
develops a more efficient root system (i.e., roots with a higher activity per
unit mass) a small root system would display a reduced ability to absorb toxic
ions and to accumulate into the shoot (Moya et al., 1999; Munns, 2002).
In C. humilis, salinity increased both Cl− and Na+ SAR (Table 2). The
root ion accumulation rate in high salinity may not be sufficient to achieve
the same ion distribution as in the control conditions. Thus, an increase
in leaf ion allocation can be achieved by an increase in leaf ion transport
rate values, JL . Since the biomass partition did not exhibit changes as a
result of salinity, a higher JL would have given rise to a higher leaf ion
concentrations. PASS-INI showed high values for both ions. PASS-DNI and
M-DRIS indicated an imbalance in both Cl− and Na+ with respect to other
 1474 M. D. Simón et al.

nutrients. In contrast, in W. robusta, the low root activity was the major factor
in controlling leaf toxic ion accumulation, since SAR and JL , of both Na+
and Cl− were reduced under saline conditions. The higher root biomass
percentage under saline conditions did not produce significant changes in
leaf ion levels and the diagnosis norms displayed normal values. These results
indicated better tolerance to potentially toxic ions in W. robusta than in C.
humilis and discount an ion-specific effect as a possible cause of the lower
relative growth of W. robusta under saline conditions (52.3% in W. robusta
and 61.9% in C. humilis) (Aljuburi, 1992).
In control conditions, both species showed leaf mineral levels that can
be considered among the lowest observed in palm trees. In fact, C. humilis
needs lower amounts of nutrients, including N, P and K, for optimal growth
compared with other palms with the lower nutrient needs (Jones et al., 1991;
Chase and Broschat, 1991).
Macronutrient SAR values were higher in W. robusta than in C. humilis in
control conditions, which suggested the presence of a higher proportion of
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young root zone in the former species (Schubert and Laüchli, 1990). In C.
humilis, salt treatment decreased about a 20% the macronutrients (N, P and
K) SAR with respect to control conditions. Decreased N uptake could be
due to an interactive effect between Na+ and NH4 + and/or between Cl− and
NO3 − at uptake sites in the roots (Hu and Schmidhalter, 2005). However,
in our study, under saline conditions, the leaf N transport rate increased
but did not significantly change leaf N concentrations. Whereas in most
cases, total N uptake (mg N per plant) decreased under saline conditions, N
concentration (mg N per kg dry weight) increased or remained unchanged
under optimal N conditions (Hu and Schmidhalter, 1998).
The availability of P may be reduced in saline soils due to ionic-strength
effects and because P concentrations in the soil solution are tightly con-
trolled by absorption and the low solubility of Ca-P minerals (Grattan and
Grieve, 1999) In C. humilis, salinity reduced leaf P transport rates and leaf P
concentrations. In cotton, salinity also inhibited P translocation from root to
shoot, inducing P deficiency in young leaves (Martinez and Laüchli, 1991).
In conclusion, since salinity did not change biomass allocation, SAR values
and plant nutrient mobilities were decisive in the leaf nutrient content.
In W. robusta, salinity reduced SAR values of N, K + and Ca2+ by about
40%. According to the model of “functional equilibrium” (Brouwer, 1963),
the increase in root biomass allocation (Table 1) suggested that nutrient
and/or water may be limiting factors in the growth of W. robusta palm trees.
The reduction in stem biomass allocation may also contribute to an increased
relative growth rate, because stems do not contribute to carbon assimilation
and the energy requirements for the formation of lignified structures is high
(Penning de Vries et al., 1974). However, considering the increase in root
biomass allocation observed, W. robusta showed good control of both Cl−
absorption and leaf Cl− accumulation.
 Nutrient Requirements under Long-Term Salt Stress 1475

Both species displayed high leaf Mg levels in saline conditions, probably

due to the high Mg2+ concentration in the irrigation water used (Simón
et al., 2010). A study by Hu and Schmidhalter (1997) revealed that leaf Mg2+
concentrations can be increased for a given salinity level by increasing Mg2+
concentrations in the nutrient solution.
The long-term responses of both palm tree species to salinity moderately
worsened the leaf nutritional balances. Both PASS-DNI and M-DRISS IN-I
showed similar values and provided essentially the same diagnoses. These
are dependent indices obtained from relationships between element con-
centrations, in the form of a ratio. Thus, they identify the order of the
limitation, but not the likelihood that a particular element is acting as a
limiting factor. In saline conditions, some nutrients showed an order of rel-
ative imbalance (P > K, N in C. humilis and N in W. robusta) while others a
surplus of nutrient (Mg in C. humilis and P in W. robusta). C. humilis showed
a higher nutrient imbalance than W. robusta with a Balance Index of 136
and 48, respectively. Leaves from C. humilis accumulated disproportionately
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higher Cl− and Na+ concentrations than those from the W. robusta. This
evoked high positive M-DRIS-IN I values, which were manifested in more
negatives DRIS indices for the other elements. By using the M-DRIS-BI ap-
proach, higher values were obtained in C. humilis than in W. robusta. One
shortcoming of this dependent nutrient index, which aims at identifying
mineral deficiencies, was that, in saline conditions, it was unable to establish
whether the nutrient deficiency was due to an excess of salinity or to bad
fertilization.
PASS norms were better at assessing nutritional deficiency in C. humilis
than in W. robusta. Thus, the ANOVA test and PASS-INI indices agree in C.
humilis (P and Mg), but not in W. robusta (N and Ca) (Table 3). Under saline
conditions, the nutrient deficiencies detected by PASS-INI (obtained from
the last two harvests) and the reductions in the time trends of JL (obtained
from all seven harvests) are in agreement. PASS-INI showed a deficiency
(<−10) of P in C. humilis (INI = −16) and another of N in W. robusta
(INI = -13), although the latter was not detected by ANOVA. Salinity reduced
the phosphorus JL with respect to the control by about 20% in C. humilis.
Under saline conditions, W. robusta there was an increase of 5.3% in the root
mass fraction, although this did not compensate fully for the decrease in
nitrogen JL of 34%. Both macronutrients are constituents of many plant cell
components and their deficiency rapidly inhibits plant growth (Marschner,
1995). A greater nutritional deficiency in C. humilis than in W. robusta was
observed in the Yield Index (68 and 16, respectively). Thus, the higher
relative biomass yield in C. humilis than in W. robusta in saline conditions
cannot be explained by an ion-specific or a nutritional effect. In a previous
paper, Simón et al. (2010) suggested that C. humilis may be more tolerant to
osmotic stress than W. robusta and that this could be the cause of the higher
relative biomass yield observed in the former.
 1476 M. D. Simón et al.

Fertilizer uptake was low in C. humilis and moderate in W. robusta com-

pared with other palm trees (Del Cañizo, 2002) (Table 4). High levels of
fertilizer could lead to a decrease in yield in salt-sensitive species due to a
sharp increase in salt concentration. In contrast, the low fertilizer require-
ments of these palm seedlings, which show moderate salt tolerance (Simón
et al., 2010), would result in a reduction of less than 0.1% in biomass yield.
The higher nutrient quantities used for W. robusta were probably due to both
higher SAR values and higher average total biomass (43.1g vs. 159.4 g). After
relating plant size to nutrient uptake, we recommend that for two-year-old
seedlings of both species only 25% of the amounts cited in Table 4 should be
used. It would be appropriate to fertilize with an N: P2 O5 : K2 O ratio of 4:1:5
in C. humilis and 5:1:3 in W. robusta. These ratios are richer in K2 O than that
proposed for palm trees by Broschat (1995; 1999). However, salinity altered
the cited ratios in both palm trees demonstrating that these plants require
an adaptation of fertilizer management in saline conditions.
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CONCLUSIONS
We conclude that both SAR and JL activity, but not biomass allocation,
were decisive as regards leaf mineral composition. PASS-INI showed a de-
ficiency (<−10) for P in C. humilis and for N in W. robusta. Under saline
conditions, PASS norms provided better diagnostic results than DRIS norms
and the former norms were better in C. humilis than in W. robusta. Nutrient
uptake was low in C. humilis and moderate in W. robusta. An appropriate
strategy would be to fertilize with an N: P2 O5 : K2 O ratio of 4:1:5 in C. humilis
and 5:1:3 in W. robusta.

ACKNOWLEDGMENTS
This work was supported by CDTI Project (IDI-20070868).

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