Universidade Federal Rural do Semi-rido ISSN 0100-316X (impresso)

Pr-Reitoria de Pesquisa e Ps-Graduao ISSN 1983-2125 (online)

http://periodicos.ufersa.edu.br/index.php/sistema http://dx.doi.org/10.1590/1983-21252017v30n220rc

PHYSIOLOGICAL RESPONSES OF DWARF COCONUT PLANTS UNDER

WATER DEFICIT IN SALT-AFFECTED SOILS1

ALEXANDRE REUBER ALMEIDA DA SILVA2*, FRANCISCO MARCUS LIMA BEZERRA3, CLAUDIVAN

FEITOSA DE LACERDA3, CARLOS HENRIQUE CARVALHO DE SOUSA3, MARLOS ALVES BEZERRA4

ABSTRACT - The objective of this study was to characterize the physiological acclimation responses of
young plants of the dwarf coconut cultivar Jiqui Green associated with tolerance to conditions of multiple
abiotic stresses (drought and soil salinity), acting either independently or in combination. The study was
conducted under controlled conditions and evaluated the following parameters: leaf gas exchange, quantum
yield of chlorophyll a fluorescence, and relative contents of total chlorophyll (SPAD index). The experiment
was conducted under a randomized block experimental design, in a split plot arrangement. In the plots, plants
were exposed to different levels of water stress, by imposing potential crop evapotranspiration replacement
levels equivalent to 100%, 80%, 60%, 40%, and 20%, whereas in subplots, plants were exposed to different
levels of soil salinity (1.72, 6.25, 25.80, and 40.70 dS m -1). Physiological mechanisms were effectively limited
when water deficit and salinity acted separately and/or together. Compared with soil salinity, water stress was
more effective in reducing the measured physiological parameters. The magnitudes of the responses of plants to
water supply and salinity depended on the intensity of stress and evaluation period. The physiological
acclimation responses of plants were mainly related to stomatal regulation. The coconut tree has a number of
physiological adjustment mechanisms that give the species partial tolerance to drought stress and/or salt,
thereby enabling it to revegetate salinated areas, provided that its water requirements are at least partially met.

Keywords: Cocos nucifera L.. Water and salt stress. Physiology.

RESPOSTAS FISIOLGICAS DE PLANTAS DE COQUEIRO ANO SOB DEFICINCIA HDRICA,

EM SOLOS AFETADOS POR SAIS

Resumo - Objetivou-se, com este trabalho, caracterizar as repostas fisiolgicas aclimatativas de plantas jovens
de coqueiro Ano, cultivar Verde do Jiqui, associadas com a sua tolerncia s condies de mltiplos
estresses abiticos (deficincia hdrica e salinidade do solo), atuando isolados e/ou combinados. O estudo foi
realizado sob condies controladas e avaliaram-se: as trocas gasosas foliares, o rendimento quntico da
fluorescncia da clorofila a e os teores relativos de clorofila total (ndice Spad). O experimento foi conduzido
sob delineamento estatstico de blocos casualizados, no arranjo de parcelas subdivididas, sendo as parcelas
constitudas por diferentes nveis de deficincia hdrica, mediante a imposio de cinco distintos percentuais de
reposio das perdas de gua por evapotranspirao potencial da cultura (100; 80; 60; 40 e 20%) e as
subparcelas constitudas pelos crescentes nveis de salinidade do solo (1,72; 6,25; 25,80 e 40,70 dS m -1). Os
mecanismos fisiolgicos so efetivamente limitados quando a deficincia hdrica e a salinidade atuam
isoladamente e/ou em conjunto. Os efeitos do estresse hdrico se mostram mais efetivos nos comprometimentos
dos parmetros fisiolgicos, em detrimento salinidade do solo. As magnitudes das respostas das plantas ao
suprimento hdrico e salinidade dependem das intensidades dos estresses e das pocas de avaliao. As
respostas fisiolgicas aclimatativas das plantas esto relacionadas, principalmente, regulao estomtica. O
coqueiro apresenta uma srie de mecanismos de ajustes fisiolgicos que conferem espcie uma parcial
tolerncia ao estresse hdrico e/ou salino, tornando-a capaz de revegetar reas salinizadas, desde que as
necessidades hdricas sejam ao menos parcialmente atendidas.

Palavras-chave: Cocos nucifera L.. Estresses hdrico e salino. Fisiologia.

____________________
*Corresponding author
1
Received for publication in 04/11/2016; accepted in 10/18/2016.
Paper extracted from the doctoral thesis of the first author.
2
Department of Education, Instituto Federal de Educao, Cincia e Tecnologia do Cear, Iguatu, CE, Brazil;
[email protected].
3
Department of Agricultural Engineering, Universidade Federal do Cear, Fortaleza, CE, Brazil; [email protected], [email protected],
[email protected].
4
National Center for Tropical Agroindustry Research, Empresa Brasileira de Pesquisa Agropecuria, Fortaleza, CE, Brazil;
[email protected].

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A. R. A. SILVA et al.

INTRODUCTION from the responses to single stress factors.

Thus, the objective of the present study was
Despite an ever-increasing need for to characterize the physiological responses of Dwarf
plant-based food, fiber, and energy, there remain coconut palm saplings (cultivar Jiqui Green)
vast areas of the world that have unfavorable associated with their tolerance to multiple abiotic
environmental conditions for plant growth. This stressors (drought and soil salinity), acting either in
includes areas in which the soil and atmosphere are isolation or in combination, to elucidate the possible
too dry and areas with high soil salinity, which are acclimatization strategies adopted by plants during
thus unsuitable for agriculture. the early stages of their growth.
Plant growth results from regulated and
integrated physiological processes (BEZERRA et al.,
2005). Drought conditions and/or salt stress are MATERIAL AND METHODS
known to induce various physiological disorders in
crops, leading to reduced growth and yields (SILVA The experiment was conducted in a
et al., 2010). greenhouse-like protected environment between
The use of plants that can tolerate high salt October 2013 and February 2014, at the
concentrations in the soil can be adopted as a Experimental Area of the Agrometeorological
strategy to transform barren areas (which are either Station of the Department of Agricultural
naturally saline, or where salinity has been Engineering, Federal University of Cear (Pici
artificially increased by inadequate management of Campus), in FortalezaCE, Brazil, with geographical
soil and water resources) into areas suitable for coordinates: Latitude 0345South; Longitude 3833
agricultural cultivation (SABRA; DAAYF; West; elevation approximately 19 m.
RENAULT, 2012). An Onset Hobo data-logger was installed in
Cultivation of coconut palm (Cocos nucifera the center of the greenhouse to characterize and
L.) occurs mainly in coastal areas, dominated by monitor environmental conditions (temperature,
"Typic Quartzipsamment" soils with sandy textures, relative humidity, and luminosity) during the course
generally characterized by their low fertility and/or of the experiment, with measurements being taken
high salinity. In the Morada Nova and every 10 min. A Class A-type tank evaporimeter
CuruPentecoste Irrigation Perimeters in the state of was also installed, with readings being performed
Cear, coconut palm is commonly cultivated in daily. The mean values of temperature, relative
"Fluvisols," which present the most varied and humidity, atmospheric water vapor pressure deficit,
diversified textural classes and degrees of salinity luminosity, and water evaporation during the
and/or sodicity; this is mainly attributable to experimental period were 29.14 2.97C,
inadequately managed irrigation and drainage 68.48% 12.60%, 3.34 1.12 kPa,
systems. Even so, coconut cultivation is an important 0.076 0.22 W m-2 (wavelength = 555 nm), and
activity in Brazil, and particularly in this region, and 5.70 0.70 mm day-1, respectively.
in recent years it has seen significant growth The experiment was conducted using a
worldwide (not just in Latin America) (SOUSA et randomized block split-plot design, with the plots
al., 2011). consisting of different water drought levels (D), by
It is assumed that coconut palm plants can imposing five percentage values of the replacement
grow in saline environments by developing a series of water loss by crop potential evapotranspiration
of adaptive physiological mechanisms, and this, in (ETpc: D1 = 100% ETpc, D2 = 80% ETpc,
concert with its economic potential, makes the D3 = 60% ETpc, D4 = 40% ETpc, and D5 = 20%
coconut palm a promising plant for cultivation in ETpc), and subplots consisting of increasing levels
salt-affected soils (LIMA, 2014; MARINHO et al., of soil salinity (S: S1 = 1.72 dS m-1,
2005). S2 = 6.25 dS m-1, S3 = 25.80 dS m-1, and
The physiological effects of drought S4 = 40.70 dS m-1). Four replicates consisting of one
(GOMES et al., 2008; GOMES et al., 2010) and plant per pot were used, for a total of
salinity of irrigation water (LIMA, 2014; 80 experimental units.
MARINHO et al., 2005) on coconut palm trees have Dwarf coconut seedlings (cultivar Jiqui
been reported previously. However, there have been Green) obtained from a certified farmer were
no reports on the mutual influence of these stressors transplanted 40 days after germination into pots with
on this plant, nor is there information available a volumetric capacity of 25 L, filled on average with
regarding the physiological responses of these trees 32.57 kg of sodic Fluvisol (S1) or sodic saline
to the mutual influence of these multiple abiotic Fluvisol (S2, S3, and S4), obtained from the topsoil
stresses. at four different sites in the Morada Nova Irrigation
Chaves, Flexas, and Pinheiro (2009) suggest Perimeter, located in the municipalities of Morada
that the physiological responses observed in species Nova and Limoeiro do Norte, in the State of Cear
induced by a combination of stressors (e.g., drought (Latitude 510South; longitude 3822West;
and salinity) are unique, and cannot be extrapolated elevation: approximately 80 m), which represented
448 Rev. Caatinga, Mossor, v. 30, n. 2, p. 447 457, abr. jun., 2017
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A. R. A. SILVA et al.

substrates with increasing salinity levels. Composite with reference to Fontes, Cintra and Carvalho-Filho
soil samples were collected from the pots to (1998), who suggest the use of 200 g of a 15:10:15
characterize their physico-hydric and chemical formulation of nitrogen, phosphorus, and potassium,
attributes, the results of which are shown in tables 1 respectively. The equivalent to 30 g of the
and 2, respectively. On the basis of these results, a commercial formulation FTE BR 12 was also
chemical correction was performed with mineral applied to meet micronutrient requirements.
fertilizers, the amounts of which were determined
Table 1. Physico-hydric attributes of soils used as substrates for the cultivation of Dwarf coconut palm saplings (cultivar
Jiqui Green).
Granulometric Composition Density Humidity
Textural class
Salinity Sand Silt Clay Soil Particles 33 kPa 1,500 kPa
(---------- g kg-1 ----------) (-) (--- kg dm-3 ---) ( ---- m m-3 ----)
S1 608 231 239 Sandy loam 1.23 2.52 19.59 12.10
S2 532 285 332 Sandy loam 1.33 2.56 19.63 11.55
S3 605 272 225 Sandy loam 1.38 2.60 17.42 9.11
S4 459 368 219 Loam 1.27 2.59 23.43 12.78
1
Table 2. Chemical attributes of soils used as substrates for the cultivation of Dwarf coconut palm saplings (cultivar Jiqui
Green)1.
pH Exchangeable cations
EC
Salinity (Water) Ca2+ Mg2+ K+ Na+ H+ + Al3+ Al3+
(-) (dS m-1) (---------------------------- cmolc kg-1 ---------------------------)
S1 6.8 1.72 6.58 4.34 0.06 4.32 2.56 0.00
S2 7.5 6.25 7.80 5.24 0.08 7.23 0.00 0.00
S3 7.4 25.80 7.51 5.69 0.05 15.78 0.00 0.00
S4 7.0 40.70 14.91 4.58 0.07 22.46 0.00 0.00
S T V ESP C O.M. Passimilable
Salinity Classification
(--- cmolc kg-1 --) (----- % -----) (---g kg-1 ---) (mg kg-1)
S1 15.30 17.86 86 24 12.26 21.13 30 Sodic
52 20.35 20.35 100 36 16.64 28.66 30 Sodic-saline
S3 29.03 29.03 100 54 9.22 15.89 69 Sodic-saline
S4 42.02 42.02 100 53 20.23 34.88 82 Sodic-saline
1 1
pH, hydrogen potential; EC, electrical conductivity of the soil saturation extract; S, sum of bases; T, cation exchange
capacity; V, base saturation; ESP, exchangeable sodium percentage; C, organic carbon; O.M., organic matter; Passimilable,
assimilable phosphorus; Classification, soil classification per salinity.
Irrigation was provided using a drip irrigation The data were submitted to analysis of
system equipped with autocompensating emitters, variance, according to a randomized block
with a nominal flow rate of 4 L h-1. The irrigation experimental design in a split-plot scheme, where the
management method was selected based on weather different drought levels were analyzed in the plots,
conditions. The methodology proposed by Bernardo, the different soil salinity levels in the subplots, and
Soares, and Mantovani (2006) was adopted to the evaluation periods of these variables in
determine the potential crop evapotranspiration sub-subplots.
(ETpc). The duration of irrigation, controlled via Significant effects were further analyzed by
independent records, was employed to differentiate regression. Upon observation of a significant effect
water stress treatments. of the interactions between the factors, multiple
The variables were analyzed at 30, 60, 90, linear regression analysis was performed and the
and 120 days after seedling transplantation (DAT). respective response surfaces were plotted.
Stomatal conductance (gs), transpiration (E), and net Mathematical models were selected based on
photosynthesis (A) measurements were performed the significances of the regression coefficients using
using a portable infrared gas analyzer (IRGA: Students t-test, of the coefficient of determination,
LCpro; ADC, Hoddesdon, UK). Chlorophyll and of the biological phenomenon being studied.
fluorescence emission was measured using a Statistical analyses were performed using Microsoft
portable modulated light fluorometer (PEA Excel software (v. 2007), ASSISTAT (v. 7.6 beta),
Hansatech, Kings Lynn, UK). The relative and STATISTICA (v. 7.0).
chlorophyll contents (SPAD index) were determined
using a portable meter (SPAD 502; Minolta Co., Ltd,
Osaka, Japan).

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RESULTS AND DISCUSSION exception being the quantum yield of chlorophyll a

fluorescence: Fv Fm-1), as indicated by the ANOVA
The variables under analysis were results shown in Table 3. Additionally, significant
significantly influenced by the following factors: effects were observed for all double and triple
drought, soil salinity, and time of evaluation (the interactions.

Table 3. Summary of the analysis of variance for stomatal conductance (gs), transpiration (E), photosynthesis (A), quantum
yield of chlorophyll a fluorescence (Fv Fm-1 ratio), and relative total chlorophyll content (SPAD index) in Dwarf coconut
saplings (cultivar Jiqui Green), grown under different levels of water stress in salt-affected soils, assessed at 30, 60, 90,
and 120 days after transplanting1.
Mean squares
SV D.F.
gs E A Fv Fm-1 SPAD index
* ** ** ns
Blocks 3 0.00144 0.26936 2.47630 0.00031 9.39ns

Drought (D) 4 0.22764** 46.08957** 518.24074** 0.00760** 62,710.32**

Residue D 12 0.00037 0.03036 0.18508 0.00132 6.43
Plots 19
Soil salinity (S) 3 0.02094** 3.49716** 36.81467** 0.00436* 4,325.10**

Interaction S D 12 0.00396** 0.25696** 1.12011** 0.00372** 777.55**

Residue S 45 0.00012 0.01072 0.10637 0.00131 1.75
Subplots 79
Time of Evaluation (E) 3 0.22495** 62.41610** 907.68968** 0.00024ns 251.71**

D E interaction 12 0.02007** 2.29278** 40.74256** 0.00439** 65.63**

S E interaction 9 0.00119** 0.04052** 2.39176** 0.00368* 4.67**

D S E interaction 36 0.00024** 0.07776** 0.64452** 0.00470** 9.64**

Residue E 180 0.00010 0.00579** 0.03389 0.00152 1.87
Total 319
C.V. - D (%) 24.24 21.40 18.72 4.65 14.47
C.V. - S (%) 13.88 16.78 16.61 4.63 12.33
C.V. - E (%) 12.36 14.98 13.73 4.99 12.41
1 1
S.V.: sources of variation, D.F.: degrees of freedom, C.V.: coefficients of variation, *: significant at 5%
probability, **: significant at 1% probability, ns: not significant by the F test.

In consideration of the specific purpose of the values were obtained with the combined use of
study, regardless of the significance of the drought 100% ETpc and the lowest salinity level
soil salinity time of evaluation interaction, the (1.72 dS m-1) (Figures 1, 2, and 3).
drought soil salinity double interaction was split. Stomatal closure is one of the fastest and
Figure 1 shows that a linear polynomial is the most intense responses that occur in plants subjected
best fit for the data, modeling the behavior of the to stressors that compromise their water status, such
stomatal conductance variable as a function of the as drought and salinity, and is considered to
level variations of the factors in the study, with a efficiently control water losses (GOMES; PRADO,
coefficient of determination (R2) of 0.9651. 2007). This stomatal response is regulated by
Application of 20% ETpc to soils with a signaling pathways that occur in roots, and is
salinity equivalent to 40.70 dS m-1 resulted in the modulated by the synthesis and distribution of
lowest values of stomatal conductance, transpiration, abscisic acid (ORSINI et al., 2012).
and photosynthesis, whereas the largest average

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Figure 1. Response surface for stomatal conductance (gs) data for Dwarf coconut saplings (cultivar Jiqui Green), in
response to combinations of different levels of water stress (% ETpc) and soil salinity levels (CE) 1.
1
(*) Significant at 5% probability using Students t-test.
Figure 1 also shows that drought levels exert excess of soluble salts, may lead to a situation
a significantly higher effect on stomatal wherein plants will lack a satisfactory suction forces
conductance, indicating thereby that drought was the to overcome this osmotic potential, resulting in an
most limiting factor to stomatal opening compared to inability to absorb water, even in moist soils.
soil salinity. This inference can be made by Silva Jnior, Passos, and Gheyi (2002) also
comparing the line slope gradients that make up the found that drought and the accumulation of salts in
response surface; those describing the drought factor soil imposed severe restrictions on stomatal behavior
are more pronounced than those of soil salinity in coconut palm plants. The authors also observed
levels. Thus, although the stomatal opening process that exposure to high salt levels reduces stomatal
is subjected to the combined influence of both opening in some salt-tolerant species and even in
stressors, it appears to be more sensitive to changes halophyte plant species, and that this in turn leads to
in water stress levels than to changes in soil salinity decreased transpiration, and consequently to reduced
levelsthe combination of 100% ETpc and primary production of photosynthates. Kusvuran
CE = 1.72 dS m-1 resulted in a mean gs value of (2012) states that high salinity has detrimental
approximately 0.32 mol H2O m-2 s-1, whereas the effects on the stomatal opening process in plants by
combination of 100% ETpc and CE = 40.70 dS m-1 increasing resistance to the diffusion of CO2.
yielded an average gs value of approximately Stomatal closure can act as an activation signal for
0.17 mol H2O m-2 s-1 (Figure 1). Similar behaviors multiple responses to stress, including inhibition of
were also observed for the transpiration (Figure 2) plant growth, which can be detrimental for yields. In
and photosynthetic (Figure 3) variables. turn, stomatal closure prevents damage to metabolic
Moreover, this behavior leads to the systems, by adjusting them to the water deficit in the
hypothesis that the effect of soil salinity may have plant (due to shortage of water and/or excess salts).
accentuated further the degree of drought stress to Our results corroborate those of Passos,
which the plants were subjected, since salts interfere Passos, and Prado (2005), who reported that under
with the water absorption capacity of the root system drought conditions during the dry season, Dwarf
(osmotic potential interference, and the reduction of coconut ecotypes respond to drought effects by
the potential gradient between soil and root cells) significantly reducing stomatal conductance. The
(KUSVURAN, 2012). The stomatal conductance effects of soil salinity levels in the present study
responses to different combinations of the stressors corroborate the findings of Lima (2014), who also
drought and soil salinity support this hypothesis. described a significant effect of irrigation water
These inferences are supported by Ramegowda and salinity on stomatal conductance. The findings of the
Kumar (2015), who state that the increased present study are also consistent with those of Silva
concentration of salts in soil solution promotes an Jnior, Passos, and Gheyi (2002), who hypothesized
increase in retention forces due to their effect on the that the coconut palm, when irrigated with saline
osmotic potential, thus amplifying the magnitude of water, has mechanisms that operate to prevent water
drought in plants. According to these authors, an stress by closing stomata, thereby substantially
increase in osmotic potential, stemming from the compromising gaseous exchange. Additionally,

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Marinho et al. (2005) found that stomatal polynomial regression analysis showed a linear
conductance in coconut palm plants decreased as the effect for the drought and soil salinity levels, as well
irrigation water salinity increased. as for the interaction between these factors, with a
The splitting of the association effects coefficient of determination (R2) of 0.9925
between treatments for the variable transpiration by (Figure 2).

Figure 2. Response surface for transpiration (E) data for Dwarf coconut saplings (cultivar Jiqui Green), in response to
combinations of different levels of water stress (% ETpc) and soil salinity levels (CE) 1.
1
(*) Significant at 5% probability using Students t-test.
As the water supply becomes limiting, dehydration, assuring survival under stress
transpiration decreases (GONALVES et al., 2010). conditions. Moreover, through stomatal regulation,
The lower transpiration values in plants under plants can prevent the incidence of several other
drought and salt stresses precisely reflect the effects signals that would further affect their respective
that such stressors exert on stomatal closure agronomical performance.
(Figure 2). This closure is the result of a reduction in According to Sabra, Daayf, and Renault
the soil's osmotic potential stemming from the (2012), plants tend to close their stomata under
increasing salt levels. This phenomenon, along with saline conditions, thus reducing the amount of
the ionic effect, may induce stomatal closure, ionic transpired water, which can contribute to a reduction
imbalance, nutritional deficiency, and consequently a in the absorption and loading of toxic ions such as
decrease in biomass production (KUSVURAN, Na+ and Cl- into their interior, thus constituting an
2012). An adequate water supply appears to mitigate additional adaptive strategy for survival under the
the effect of salinity on the transpiration rates, i.e., predominance of these stressful conditions. Hence,
results in smaller decreases (Figure 2). the inferences described above can explain plant
It should be noted that the lowest survivability based upon an association between
transpiration values were observed for the ETpc- and CE-stressing agents, assuming that the
combination of treatments that also resulted in the regulation of stomatal opening, and consequently
lowest values of stomatal conductance. This direct control of water loss, is a mechanism adopted by
correspondence between stomatal conductance and plants to adjust to adverse conditions (CHAVES;
transpiration is expected, taking into consideration FLEXAS; PINHEIRO, 2009). These assertions are
the fact that stomatal closure reduces water vapor corroborated by Sucre and Surez (2011), who
outflow into the atmosphere (and consequently also hypothesized that plants respond to drought and
reduces transpiration rates) (GONALVES et al., salinity by closing stomata, thus reducing leaf
2010). transpiration and/or preventing the development of
The present results indicate that the reduction an excessive water deficit situation in tissues. This
in stomatal conductance and transpiration can response enables the leaf to retain a water potential
partially compromise photosynthetic activity. When capable of maintaining its adjustment to and/or
plants were exposed to different levels of salinity, recovery from stressor-induced damage, whether
transpiration rate decreases were estimated to be these stressors act in isolation or in combination.
1.08%, 0.72%, 0.38%, 0.30%, and 0.20% per unit Regarding photosynthesis, the proposed
increase of CE, and in ETpc replacement levels model indicates that drought and soil salinity effects
equivalent to 20%, 40%, 60%, 80%, and 100%, increase and reduce photosynthetic rates,
respectively (Figure 2). However, Orsini et al. respectively, and can be described using a linear
(2012) inferred that such responses can also be polynomial with a coefficient of determination (R2)
viewed as a means of protecting plants from rapid of 0.9866 (Figure 3).
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Figure 3. Response surface for photosynthesis (A) data for Dwarf coconut saplings (cultivar Jiqui Green), in response to
combinations of different levels of water stress (% ETpc) and soil salinity levels (CE) 1.
1
(*) Significant at 5% probability using Students t-test.

In the present study, the highest effects such as increased resistance to internal
photosynthetic rates were obtained with a drought transport of CO2, damage to the photosynthetic
control level of 100% ETpc and the lowest salinity machinery caused by stressors, biochemical
level (1.72 dS m-1). Conversely, the lowest alterations that can directly compromise the
photosynthetic rates were measured when a drought photosynthetic efficiency, and even salt effects on
level corresponding to 20% of ETpc in association chloroplasts (particularly on the transport of
with the highest level of soil salinity (40.70 dS m-1) electrons and on the secondary processes), may also
were imposed; the extent of reduction was extremely have occurred. Furthermore, a decrease in
dependent on the intensity of drought and salt levels photosynthesis under stress conditions can also stem
(Figure 3). This behavior contrasts with the from leaf size reduction (SANTOS et al., 2012).
observations reported by Sucre and Surez (2011), According to Gomes and Prado (2007),
wherein some studies showed that plant survivability drought-induced reductions in photosynthetic rates in
capacity increases when affected by a combination coconut palm plants are initially ascribed to a
of salinity and drought, i.e., compared to situations limitation in CO2 diffusion from the atmosphere into
in which the plants are only affected by drought or the intercellular spaces as a result of stomata closure.
salinity alone, plant physiology is less compromised. The authors also observed that factors unrelated to
Thus, the general trends shown in the present study stomata contribute to a reduction in photosynthesis,
support the hypothesis that stressor combinations both during a period of severe drought and during
may potentiate the effects of their action when acting the recovery phase after water supply is resumed.
alone (CHAVES; FLEXAS; PINHEIRO, 2009). Indeed, during the latter, factors unrelated to stomata
Similar to the observation on cashew plants are more relevant to photosynthetic modulation.
reported by Bezerra et al. (2005), it is assumed that According to Sabra, Daayf, and Renault
much of the reduction in photosynthesis in coconut (2012), the non-stomatal factors potentially capable
plants stems from stomatal limitation. Silva et al. of restricting photosynthetic activity are biochemical
(2010) reported similar results in Jatropha plants, in nature, and include the inhibition of Rubisco
which also exhibited a strong restriction of activity and ATP synthesis; these responses are
photosynthesis via stomatal closure, as a prevention complementary to the stomatal responses to stress in
strategy for both stress conditions (drought and plants.
salinity). Silva et al. (2011a) also reported a decrease The water favoritism, conditioned by
in photosynthesis, associated with low leaf stomatal increasing levels of ETpc, promoted an increase in
conductance in plants simultaneously subjected to the Fv Fm-1 ratio. However, the magnitude of the
salinity and drought. response was restricted by the influence of
Although a decrease in photosynthesis is increasing soil salinity (Figure 4).
mostly due to a decrease in stomatal conductance,

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Figure 4. Response surface for chlorophyll a fluorescence quantum yield (Fv Fm-1 ratio) data for Dwarf coconut saplings
(cultivar Jiqui Green), in response to combinations of different levels of water stress (% ETpc) and soil salinity levels
(CE)1.
1
(*) Significant at 5% probability using Students t-test.

Generally, and consistent with the findings of in the Fv Fm-1 ratio when plants are subjected to a
the study by Silva et al. (2014) on citrus hybrids, the given stressor is related to photoinhibitory effects,
quantum yield of chlorophyll fluorescence upon and can represent either a reversible photoprotective
imposition of saline stress responds in a manner regulation or an irreversible inactivation of PS2. For
similar to the variables related to gas exchange in these authors, the implications arising from the
leaves. When we analyzed the effect of salinity in effects of drought on this variable show that plants
isolation, we found that our results differ from those often exhibit a remarkable inhibitory effect on
obtained by Marinho et al. (2005), who found that photosynthesis, which is characterized by a
the salinity of the irrigation water did not affect significant decrease in PS2 quantum yield. Gomes et
variables pertaining to the efficiency of the al. (2008) also observed a decrease in Fv Fm -1 ratios
photosynthetic machinery in coconut palms, at any of two coconut palm ecotypes grown under
given evaluation point of that assay. However, our conditions of water scarcity, which led to the
results are similar to those obtained by Lima (2014), assumption that water stress causes photoinhibition
who also observed decreases in the Fv Fm-1 ratio in coconut genotypes. According to the authors, in
when coconut palms were subjected to irrigation addition to high irradiation, any environmental
with saline water. restriction that can directly or indirectly limit the
According to Azevedo Neto et al. (2011), the photosynthetic capacity is potentially capable of
Fv Fm-1 ratio is an estimate of the maximum inducing photoinhibition. Moreover, corroborating
quantum efficiency of the photochemical activity of Arajo et al. (2010), the authors also hypothesize
photosystem II (PS2) when all its reaction centers that decreases in Fv Fm-1 ratios can actually reflect
are open. Disturbances in this ratio are ascribed to certain photochemical adjustments that plants may
salinity stress effects on the photosynthetic system, adopt under adverse weather and soil conditions, and
considering that its reduction suggests a decline in is not a consequence of damage to PS2, noting that
the photochemical efficiency of PS2, in addition to the decrease in the Fv Fm-1 ratio can result from an
indicating the occurrence of disturbances and/or increase in the initial fluorescence (Fo). This finding
damage to the photosynthetic machinery in response is consistent with that of Cruz et al. (2009), who
to the inherently adverse salinity effects. reported that an increase in Fo causes increased loss
Furthermore, considering that the values obtained for of excitation energy during its transfer among
the Fv Fm-1 ratio when plants were subjected to the antenna pigments and reaction centers, and thereby
combination of the most severe drought level (20% constitutes a factor that contributes significantly to a
ETpc) and the lowest salinity level (1.72 dS m-1) decrease in the Fv Fm-1 ratio.
were lower than those obtained for plants subjected According to Gonalves et al. (2010), there is
to the combination of full water supply (100% ETpc) no consensus in the literature regarding what effects
and the highest salinity (40.70 dS m-1), it can be a decrease in soil water availability may produce on
reasoned that drought conditions exerted a more the Fv Fm-1 ratio. Some authors state that, in general,
pronounced effect, in such a way that adequate water plants show a rapid decrease in the ratio when the
supply appears to mitigate the adverse effects of water content in soil is reduced, whereas others
salinity in the photosynthetic apparatus (Figure 4). argue that the electron transport capacity is not
According to Arajo et al. (2010), a decrease altered by water stress, which reflects the invariance

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 PHYSIOLOGICAL RESPONSES OF DWARF COCONUT PLANTS UNDER WATER DEFICIT IN SALT-AFFECTED SOILS

A. R. A. SILVA et al.

of the Fv Fm-1 ratio under drought predominance. efficiency, since values below 0.75 indicate a
Although statistically significant, the differences in reduction of the photosynthetic potential of plants
Fv Fm-1 ratios between the different levels of due to the incidence of certain forms of stress,
drought and soil salinity observed in the present whereas the capability of maintaining a high Fv Fm -1
study were relatively small and independent of the ratio (>0.80) indicates a highly efficient use of
time of evaluation. In general, their values fell within radiation by carbon assimilation reactions, despite
the range 0.491.00, with an overall mean value of the prevalence of conditions that are adverse to
0.78 0.04, which indicates that some of the plants.
combinations between the studied factor levels at Through the response surface study for the
different evaluation times resulted in damage to the variable relative total chlorophyll content (SPAD
PS2 reaction centers, as shown in Figure 4. Such index), the highest values were obtained under full
inferences are based on the findings of Silva et al. irrigation conditions (100%), whereas the lowest
(2013), who stated that the Fv Fm-1 ratio should values were observed under the most severe level of
always be approximately 0.8 for satisfactory drought stress (20% ETpc), as shown in Figure 5.

Figure 5. Response surface for relative total chlorophyll content (SPAD index) data for Dwarf coconut saplings (cultivar
Jiqui Green), in response to combinations of different levels of water stress (% ETpc) and soil salinity levels (CE) 1.
1
(*) Significant at 5% probability using Students t-test.
Therefore, it can be inferred that an increase readings reflect decreases in chlorophyll content, as
in the SPAD index with increasing water supply is a a response to salt stress (SILVA et al., 2011a). These
clear reflection of the sensitivity of relative authors speculate that this behavior may be
chlorophyll contents in coconut plant saplings to associated with the degradation of chlorophyll
water stress. This is consistent with the findings of pigments through increased chlorophyllase activity
Silva et al. (2011b), who showed that drought stress and instability of the protein complex under salt
is typically characterized by a loss of chlorophyll, stress. However, the authors also argue that instead
associated with a progressive decline in the of chlorophyll degradation, this decrease could be
photosynthetic capacity of plants. This behavior can attributed to the influence of ions on the synthesis of
be explained by the more prominent effect caused by new proteins that are structural components of
drought on this variable, coupled with the likely chlorophylls.
ability that an adequate water supply has in Generally, SPAD index values for the
mitigating the potential adverse effects that salinity different combinations between treatments ranged
alone could exert on total chlorophyll content. This between 13.4 and 134.1 SPAD units, with an overall
is based on the observation that an increase in water average value of 56.7 24.0 SPAD units (Figure 5).
availability yielded higher chlorophyll values, and Given that the lowest values were obtained with
that the intensity of the response variable was combination treatments that represented the most
compromised as a result of the adverse effects of severe stress levels, it can be deduced that, among
salinity. other causes, the prevalence of these conditions
According to Chaves, Flexas, and Pinheiro affected the photosynthetic process due to the onset
(2009), the interactions between stressors in plants of a chlorophyll deficit. According to Torres Netto et
may retard, disguise, or even transform the plants al. (2005), this aspect becomes clear among different
responses to an isolated stress factor. Lima (2014) plant species showing SPAD index readings below
found significant linear reductions in relative total 40 SPAD units. These results corroborate the
chlorophyll contents with increasing salinity in information reported by Cardoso et al. (2011) on the
irrigation water. The decreases in SPAD index existence of factors that may influence SPAD

Rev. Caatinga, Mossor, v. 30, n. 2, p. 447 457, abr. jun., 2017 455
 PHYSIOLOGICAL RESPONSES OF DWARF COCONUT PLANTS UNDER WATER DEFICIT IN SALT-AFFECTED SOILS

A. R. A. SILVA et al.

readings, such as environmental conditions UFV, 2006. 625 p.

(temperature, light, water stress, soil salinity, etc.),
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Higher Education Personnel (CAPES), National 379-384, 2010.
Counsel of Technological and Scientifc
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Science and Salinity Technology (INCTSal) for the leaves of young Brazilian Green Dwarf coconut
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