the effect of reducing soil water

Acta Oecologica 107 (2020) 103617
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Acta Oecologica
journal homepage: www.elsevier.com/locate/actoec
The effect of reducing soil water availability on the growth and
reproduction of a drought-tolerant herb
Bruno Ayron de Souza Aguiar a, *, Elda Simone dos Santos Soares a,
~o Fraga dos Santos b,
Vanessa Kelly Rodrigues de Araujo a, Josiene Maria Falca
Danielle Melo dos Santos c, Andr�e Maurício Melo Santos c, Kleber Andrade da Silva a, b,
Jefferson Thiago de Souza d, Elcida de Lima Araújo a, e
a
Universidade Federal Rural de Pernambuco, Departamento de Biologia, Programa de P�
os-Graduaç~
ao em Bot^
anica, Rua Manoel de Medeiros s/n, Dois Irm~
aos, Recife,
PE, Brazil
b
Universidade Estadual de Alagoas, Núcleo de Biologia, Rodovia Eduardo Alves da Silva, Km 3, Bairro Graciliano Ramos, Palmeira dos índios, AL, Brazil
c
Universidade Federal de Pernambuco, Centro Acad^emico de Vit�
oria (CAV), Rua Alto do Reservat�
orio, s/n, Bela Vista, Vit�
oria de Santo Ant~
ao, PE, Brazil
d
Universidade Estadual do Cear�
a, Faculdade de Educaç~
ao, Ci^encias e Letras de Iguatu (FECLI), Av. D�
ario Rab^elo, s/n, Vila Santo Ant^
onio, Iguatu, CE, Brazil
e
Universidade Federal de Pernambuco, Centro de Bioci^encias, Av. Prof. Moraes Rego, 1235, Cidade Universit�
aria, Recife, PE, Brazil
A R T I C L E I N F O
A B S T R A C T
Keywords:
Water deficiency
Plant growth
Phenology
Semi-arid
Flower
Soil water availability in the dry tropical forest varies depending on the rainfall heterogeneity, which may be
altered by future climate changes. The predicted water restrictions may modify the strategies of the herbaceous
component in the allocation of resources jeopardizing their survival. We aimed at knowing the vegetative,
reproductive and phenological responses of Talinum paniculatum under simulated conditions of reduced soil
water supply. It is a drought-tolerant herb used in traditional medicine, such as non-conventional plant food and
animal fodder. A total of 150 individuals of the herb were submitted to three treatments of water deficiency:
T100 (control; 100% field capacity - FC), T50 (50% FC), and T25 (25% FC), with 50 replicates per treatment.
Plant growth and reproduction were monitored and differences were tested using General Linear Models. In T50
there was a decrease in diameter growth and in the production and morphometry of flowers, fruits, and seeds, as
well as delays in plant phenology, not interfering with leaf production and growth in height. Reduction in
anthesis time and change in flower staining were verified in T50. There was a total absence of flowering and
fruiting in T25, besides the drastic reductions in growth. In general, we suggest that increasing soil water re­
strictions may be negative for herb growth and reproduction, but we do not rule out that reductions in attributes
can be considered as water-saving strategies. However, the predicted effect of reducing rainfall in dry forests will
compromise the reproductive success and population growth of a drought-tolerant herb.
1. Introduction
In semi-arid environments, temporal and spatial heterogeneity of
water availability (Asbjornsen et al., 2011; Albuquerque et al., 2012;
Zeppel et al., 2014) influence the manifestations of vegetative and
reproductive phenological events of plants (Morellato et al., 2013;
Richardson et al., 2013). Although many species adjust to rainfall
rhythm variations (Jongen et al., 2015), climate change, including
prolongation and intensity of rainfall reduction, can lead to changes in
the duration of phenophases, as well as quantitative declines in the
production of flowers, fruits, and seeds (Becerra, 2014; Miranda et al.,
2014; Yousfi et al., 2015), affecting the annual renewal of herbaceous
populations (Araújo et al., 2007; Silva et al., 2015).
Changes in water availability can cause drastic reductions in the
growth of expansion tissues (Miranda et al., 2009; Bernal et al., 2011; Xu
et al., 2010; Muller et al., 2011; Tardieu, 2014), affecting the carbon
accumulation in the plant (biomass) (Correia et al., 2016). In general, in
response to water deficiency, plants can: a) present adjustment strate­
gies with changes in physiological and phenological processes to tolerate
deficiency, often exhibiting complete deciduous in the dry period (Oli­
veira et al., 2015), b) adopt drought escape strategies, as occurs with
terophytes that complete the entire life cycle in the rainy season (Araújo
* Corresponding author.
E-mail addresses: [email protected], [email protected] (B.A.S. Aguiar).
https://doi.org/10.1016/j.actao.2020.103617
Received 19 May 2019; Received in revised form 23 May 2020; Accepted 9 June 2020
Available online 21 July 2020
1146-609X/© 2020 Elsevier Masson SAS. All rights reserved.
B.A.S. Aguiar et al.
Acta Oecologica 107 (2020) 103617
et al., 2005; Moreno et al., 2008; Tardieu, 2014), and c) present evasion
responses, as occurs with geophytes that store nutrients in their roots
and remain in latency in soil during the dry period (Moreno et al., 2008;
Khodorova and Boitel-Conti, 2013).
However, even during the rainy season, the distribution of rainfall
can be very irregular, and it would rain below or above the normal
average of the region, as well as the absence of rainfall for consecutive
days, interrupting the rainy signal to the plants (Sharp et al., 2009; Xu
et al., 2010; Miranda et al., 2014). Such irregularities are stochastic and
affect plant development, especially in the case of newly germinated
seedlings (Araújo et al., 2007; Becerra, 2014; Silva et al., 2015), and a
tradeoff may occur between phenotypic plasticity of ecophysiological
attributes of the plants and their survival under drought conditions
(Bongers et al., 2017; Lambrecht et al., 2017). In addition, the annual
variation in total rainfall affects the occurrence of some annual species
(Reis et al., 2006; Silva et al., 2015), which may account for 48% of the
species richness stored in the soil bank of the forests of some semi-arid
environments (Santos et al., 2013b). Studies describing the responses
of plants from semi-arid environments to a simulated reduction of water
availability show low productivity (Miranda et al., 2009; Correia et al.,
2016; Gibson-Forty et al., 2016), flowering delays, and biometric vari­
ations of the reproductive aspects (flowers, fruits and seeds) (Prieto
et al., 2008; Crimmins et al., 2010; Miranda et al., 2014), and such re­
sponses are expected to occur in natural habitats as well.
Predictive studies of the climate changes show that drought severity
in tropical forests will increase as a consequence of global warming
processes (Vicente-Serrano et al., 2013; Dai, 2013; IPCC, 2014). By the
end of the century, it will reduce the occurrence of rainfall between 30%
and 70% in the Caatinga, a Brazilian dry tropical forest. It is believed
that such changes can trigger the desertification process of this vegeta­
tion formation (PBMC et al., 2014), which will reduce the survival
chances of herbaceous plants, a dominant component of these regions.
In light of this evidence, it is of fundamental importance to monitor
herbaceous growth and reproduction in simulations of soil water con­
straints, in order to understand the functioning of forests in semi-arid
environments. Such experiments may reflect reality and provide a
broad view of how ecosystems will respond to these anticipated climate
changes (Knapp et al., 2018).We hypothesized that delays in pheno­
logical rhythm and reductions in vegetative and reproductive growth of
Talinum paniculatum (Jacq.) Gaertn (Talinaceae) plants occur as soil
water availability decreases. We use the perennial herb as a model
because it has adaptive traits to tolerate drought conditions (Guerere
et al., 1996), besides its wide distribution in dry tropical forests (Men­
doza and Wood, 2013), creating abundant populations in the Caatinga
vegetation (Santos et al., 2013a). Specifically, we answer the following
questions: 1) What happens to the vegetative and reproductive growth
of a drought-tolerant herb if there is a 50% and 75% reduction in water
availability in the soil? 2) Are the synchrony and the vegetative and
reproductive phenological rhythm from the studied herb altered by
reducing soil water availability?
fodder (Santos et al., 2010; Tolouei et al., 2019; Souza et al., 2020). Its
reproduction can be crossed or by self-pollination, being considered
facultative autogamous, with barochoric dispersion and seeds that pre­
sent dormancy (Valerio and Ramírez, 2003; Mendoza and Wood et al.,
2013). For this study, the seeds of T. paniculatum were collected from an
abundant population in the Caatinga vegetation of the Instituto Agro­
^mico de Pernambuco - IPA (8� 140 1800 S; 35� 550 2000 W; semi-arid
no
climate (BSh); 535 m height; average temperature: 22,7 � C; average
relative humidity: 51,7; average annual rainfall: 662.3 mm), located in
Caruaru (PE), Brazil (Reis et al., 2006; Santos et al., 2013b). Seeds were
collected from different individuals during the rainy season, usually
between March and August.
2.2. Experimental conditions
Initially, seeds were sanitized with 2.5% sodium hypochlorite and
scarified with the use of 100% sulfuric acid (H2SO4) for 10 min, and then
submerged in water for 24 h to overcome dormancy. This treatment was
selected because it presented a better germination result among 4
treatments applied in a germination pre-test (Souza et al., 2020). Sub­
sequently, seeds were placed to germinate in Petri dishes, containing
previously moistened filter paper. The plates were maintained in a BOD
chamber at 25 � C temperature, with 24-h photoperiod. Ten days after
germination, 150 seedlings with healthy visual aspects were carefully
transferred to properly labeled polyethylene bags containing 2 kg of
autoclaved soil [sandy loam soil from the same site of seed collection;
Soil texture: sand (19%), clay (69%), silt (12%); pH: 5.5; soil chemistry
(ppm): K (27.6), P (12), Na (23.2), Fe (52)]. Before transplanting the
seedlings, we determined the field capacity (FC) by the gravimetric
method, and soil water content (w) in 10 2 kg soil samples, transforming
the average obtained values in percentage (Cassel and Nielsen, 1986;
Assi et al., 2018). The transplanted seedlings were kept in a greenhouse
for 15 days for acclimatization under the following conditions: total
exclusion of rainfall; 100% FC; average natural daylight: 240.33 μmol
m 2 s 1; average temperature: 28.7 � C; relative humidity: 64.8%.
After the acclimation period, the seedlings were submitted to three
treatments (T) of water deficiency, T100: 100% FC - control (w ¼
17.5%), T50: 50% FC (w ¼ 8.75%), and T25: 25% FC (w ¼ 4.37%), and
monitored during 6 months, until complete maturation. The duration of
the experiment was based on the period of growth and reproduction of
herbaceous plants, which occur during the rainy season of the region
(March to August), where 82% of rainfall is concentrated. For delin­
eating the percentage of water reduction in the soil, we considered 60
years of historical data (1957–2016) provided by IPA. These reports
show that, in the Caatinga fragment, the driest year from the last 60
years (1993), had about 70% reduction of rainfall amount when
compared to the year with heavier rainfall (2004). Due to the irregular
distribution of annual rainfall, this may represent a reduction of more
than 70% (25% CP) of the available water amount in forest soil in drier
years. This effect may be more severe considering the predictions of up
to 70% reduction in rain occurrence by the end of this century in the
Caatinga (PBMC et al., 2014).
The experimental design was completely randomized, with 50 rep­
licates per treatment. Initially, 30 seedlings were labeled and separated
to monitor and quantify vegetative growth, flower, fruit, and seed pro­
duction, as well as to monitor phenological behavior. The remaining 20
seedlings were marked and separated for destructive for collection,
aiming at monitoring and quantifying the effect of water deficiency on
the morphometric traits of flowers and fruits. To maintain the water
levels established in each treatment, the bags were weighed daily and
the amount of lost water was restored.
2. Material and methods
2.1. Studied species and seeds collection
Talinum paniculatum (Jacq.) Gaertn (Talinaceae) was selected as a
model to understand the effects of water deficiency on growth and
phenological responses, because it belongs to the herbaceous component
that presents high species richness in semi-arid environments, such as
the Caatinga in Northeast Brazil. It is a geophyte (perennial herb) that
presents leaf and stem succulence, and roots that store nutrients and a
C3/crassulacean acid metabolism (CAM) photosynthetic pathway, traits
that are considered as adaptations to drought (Guerere et al., 1996;
Landrum, 2002; Santos et al., 2013a; Assaha et al., 2017). The herb is
used in many parts of South America, Africa and Asia in traditional
medicine, in human food (non-conventional plant food) and as animal
2.3. Monitoring of vegetative and reproductive attributes
Growth in height, diameter, and cumulative leaf production was
measured weekly in thirty (30) plants per treatment. The stem diameter
2
B.A.S. Aguiar et al.
Acta Oecologica 107 (2020) 103617
measurement site was marked with ink at the time of the first mea­
surement. The other diameter measurements were made at the same
marked site. In addition, 30 leaves were monitored from the beginning
of sprouting to abscission to determine longevity and leaf expansion
(leaf length and width). At the end of the six months monitoring, another
leaf per plant and treatment (healthy and still expanded) was collected
and scanned to measure the total leaf area (TLA), with the aid of the
software Image pro plus 7.0. All morphometric measurements were
performed using a tape measure and a digital caliper. From these values,
we determined the physiological indexes such as the relative growth rate
(RGR), height (RGRh), diameter (RGRd), leaf length (RGRll) and leaf
width (RGRlw) (unit: mm mm 1 week 1), using the following formula:
RGR ¼ (lnW2-lnW1)/(T2-T1), where “lnW2” and “lnW1” are the loga­
rithm Neperian of the value of the attributes per plant at times “T100 and
“T2” (weekly) (Radford, 1967; Duncan and Hesketh, 1968).
To evaluate the total leaf production (TLP), we adapted the foliar
gain formula (FG ¼ LNf - LNi; FG - foliar gain; LNf - final leaf number;
LNi - leaf number initial) according to Bugbee (1996). We calculated the
“TLP” by adding all the “FG” obtained in each week, and for this only the
positive values (>0) were used, since the negative values represent the
loss of leaves.
The reproductive attributes monitored were the number of flowers,
fruits, seeds, and the morphometry of flower and fruit structures. The
number of flowers and fruits was counted daily from the start of flow­
ering on the 30 plants marked by treatment. The total number of seeds
produced was estimated from 120 randomly selected fruits per treat­
ment. At the end of the six months, the viability of produced seeds was
evaluated through the germination test, using 60 seeds per treatment,
previously scarified with sulfuric acid and submerged in water for 24 h.
The fruit/flowers and seeds/fruits ratios of each treatment were
measured using the values of the total production.
From the 20 separate plants we collected: a) a sample of 90 fruits (30
per treatment) to measure the morphometric data (diameter and
weight), using a digital caliper and an analytical precision scale; and b) a
sample of 90 open flowers (30 per treatment) to quantify the morpho­
metric data of the floral parts, measuring the length and width of the
petals, sepals, pistils, and stamens, with the aid of a digital caliper.
Additionally, in each treatment, 100 pre-anthesis flower buds were
marked to observe the anthesis duration process. Morphometric mea­
surements of vegetative and reproductive growth were made using the
methodologies proposed by Cornelissen et al. (2003) and
P�erez-Harguindeguy et al. (2013).
correlation between mean and variance. To analyze the phenological
time series, we used circular statistics following Morellato et al. (2010):
a) the weeks and days, depending on the observation interval, were
converted into angles (vegetative phenology: 14.4� ¼ 1st week to 360�
¼ 25th week, an interval of 14.4� ; reproductive phenology: 2.14� ¼ 1st
day to 360� ¼ 168� day, an interval of 2.14� ), b) the period of greatest
phenological activity was defined based on the mean angle (μ), c) the
significance of the mean angle was verified by the Rayleigh Test (Z),
which indicates seasonality in phenological events, d) the degree of
seasonality was determined by the length of the mean vector (r), and e)
differences between treatments and peak activity were assessed by the
Watson-Williams test (F test). All analyses were performed using Sta­
tistic 7.0 (StatSoft Inc, 2004) and Oriana 4.2 software (Kovach, 2011).
3. Results
3.1. Vegetative growth
All vegetative attributes of T. paniculatum differed significantly
among treatments (RGRh: F ¼ 89.13; p < 0.01; RGRd: F ¼ 63.19; p <
0.01; RGRll: F ¼ 716.88; p < 0.01; RGRlw: F ¼ 787.81, p < 0.01, TLA: F
¼ 110.96, p < 0.01, and TLP: F ¼ 55.03, p < 0.01) (Fig. 1; Fig. 2a;
Table 1). However, the RGRh and TLP did not show significant differ­
ences between T100 (control) and T50, but both differed from T25 (p <
0.05). The highest TLP was verified in T50. In average, plant growth
among treatments was quantitatively different from the 8th week. The
highest water restriction (T25) resulted in low growth without signifi­
cant variations during the monitored time.
In response to the water reductions of T50 and T25 treatments, plants
presented the following reduction percentages in vegetative growth:
height (11.38% and 84.98%), leaf length (29.20% and 76.56%), leaf
width (26.29% and 70.56%), and leaf area (29.59% and 80.65%).
However, in relation to diameter and leaf production, there was a
divergence in plant responses, with an increase in T50 of 4.14% and
7.91% for diameter and accumulated leaves production, and a respec­
tive reduction of 58.72% and 56.33% in T25. GLM analysis showed that
about 54%–71% of vegetative growth was explained by the reduction of
soil water availability (Table 1).
3.2. Reproductive growth
There were significant differences in the production of flowers (F ¼
32.97, p < 0.01), fruits (F ¼ 35.06, p < 0.01), and seeds (F ¼ 42.99, p <
0.01) (Fig. 2b, c, d; Table 1). In the control, plants produced 4348
flowers, 1600 fruits, and 25,871 seeds. This production fell to 1705
flowers, 645 fruits and 7967 seeds in T50, and it was null in T25.
Therefore, in response to a 50% reduction of water supply, plants pre­
sented a reduction of 60.8% in flower production, 59.7% in fruit pro­
duction and 69.3% in seed production. In T25 water reduction plants did
not reproduce.
T. paniculatum produced many flowers per inflorescence in T100
(control) and T50, but few fruits were formed, despite its facultative
autogamy. As a result, the fruit/flower ratio was low in control (0.36)
and practically equal to T50 (0.37). The seed/fruit ratio was 15.77 in the
control and 12.33 in T50. The floral anthesis lasted 5 h (12 h–17 h) in the
control, but most of the plants (74%) of the T50 anticipated the begin­
ning and the end of the anthesis in 1 h.
The morphometric variations of the reproductive structures differed
statistically between the treatments in petal lengths (F ¼ 593,47, p <
0.01), sepals (F ¼ 432,62, p < 0.01), pistils (F ¼ 313, 09, p < 0.01), and
stamens (F ¼ 535.78, p < 0.01), petal widths (F ¼ 328.08, p < 0.01),
sepals (F ¼ 269.70, p < 0.01), fruits weight (F ¼ 279.4, p < 0.01) and
diameter of fruits (F ¼ 1659, p < 0.01) (Fig. 1, Table 1). The flowers
showed pink-purple coloration in the control treatment, but in T50 they
presented a paler pink or mauve rosy-pink color.
In T50 plants had the following percentages of morphometry
2.4. Phenological behavior monitoring
In the 30 plants selected by treatment, a weekly monitoring of the
occurrence of vegetative phenophases (budding, senescence, and foliar
abscission), was carried out, and reproductive phenophases (flowering,
fruiting, and dehiscence of fruits) was daily monitored. The activity
index was measured to describe the rhythm and phenological synchrony
of the populations, and it is expressed by the number of individuals that
were simultaneously manifesting a certain phenological event, consid­
ering only the presence (1) or absence (0) of the phenophases. The
phenological event was considered as non-synchronous or asynchronous
when up to 20% of the marked plants exhibited the monitored pheno­
phase, synchronic or low synchrony when more than 20% and less than
60% of the plants exhibited the phenophase, and highly synchronic
when more than 60% of the plants exhibited the phenophase (Bencke
and Morellato, 2002; Morellato et al., 2010).
2.5. Statistical analysis
The explanatory power of the water factor and the differences in the
vegetative and reproductive attributes among the water availability
treatments were evaluated by GLMs (General linear model), incorpo­
rating an ANOVA, with Tukey a posteriori test, because there was no
3
B.A.S. Aguiar et al.
Acta Oecologica 107 (2020) 103617
Fig. 1. Effect of simulated reduction of soil water availability on the vegetative and reproductive morphometric aspects of Talinum paniculatum (Jacq.) Gaertn.
Differential letters among water availability treatments, indicated by field capacity (FC), denote significant differences by the Tukey a posteriori test. T: treatments;
T100: 100% FC, T50: 50% FC, T25: 25% FC; Relative growth rate (RGR) in height (RGRh), diameter (RGRd), leaf length (RGRll), leaf width (RGRlw); total leaf
production (TLP).
Fig. 2. Effect of simulated reduction of soil water availability on the production of (a) leaves, (b) flowers, (c) fruits, and (d) seeds of Talinum paniculatum (Jacq.)
Gaertn. Differential letters among water availability treatments, indicated by field capacity (FC), denote significant differences by the Tukey a posteriori test (T:
treatments; T1: 100% FC, T2: 50% FC, T3: 25% FC).
reduction (in relation to the control) of their flowers and fruits: length of
petals (40%) and sepals (31.6%); width of petals (41.8%) and sepals
(24.1%); length of stamens (19.1%) and pistils (26.7%); diameter
(11.28%) and weight (13.02%) of the fruits. GLM analysis showed that
about 41%–97% of reproductive growth was explained by the reduction
of soil water availability (Table 1).
3.3. Plant phenology
The vegetative and reproductive phenological rhythm presented a
seasonal trend (Z > 49.2, r > 0.6, p < 0.01), with a definite direction in
the monitoring period, except for leaf budding (Z ¼ 0.2, r > 0.1, p >
0.05) that was a uniform event (Fig. 3a; Table 2). The phenophases of
leaf senescence (F ¼ 1.656, p ¼ 0.19) and foliar abscission (F ¼ 0.331, p
¼ 0.73) did not differ among the activity peaks, but the T25 budding
differed significantly from the other treatments (F ¼ 50.95, p ¼ 0.04)
4
B.A.S. Aguiar et al.
Acta Oecologica 107 (2020) 103617
Table 1
GLM analysis (linear generalized model) showing the influence of simulated reduction of soil water availability on vegetative, reproductive and phenological responses
of Talinum paniculatum (Jacq.) Gaertn.
Attributes/Phenophases
DF
SS
SST
Error
MS
F
P
R2
RGRh
RGRd
RGRll
RGRlw
TLA
TLP
flowers production
fruits production
seeds production
petals lenght
sepals lenght
petals width
sepals width
stamens lenght
pistils lenght
diameter of fruits
fruits weight
flowering
fruiting
dehiscence of fruits
foliar budding
foliar senescence
foliar abscission
2
2
2
2
2
2
2
2
2
2
2
2
2
2
2
2
2
2
2
2
2
2
2
0.23
0.02
0.08
0.06
6966
22587.2
372759
45499
11703696
187.57
65.41
77.93
35.05
94.45
72.22
205.5
0.002
100089
159366
4368
3144
1161
18.97
0.33
0.03
0.11
0.09
9697
40440.1
864462.1
101945.6
23545908
196.5
84.7
69.72
38.76
99.48
78.80
210.92
0.002
162909.7
260322.3
9731.88
10774.64
14586.19
3517.48
0.11
0.01
0.03
0.02
2781
17852.8
491703.2
56446.1
11842213
9.0079
6.77
4.30
3.7
5.02
6.57
5.38
0.0003
62820.7
100955.8
5363.56
7630.57
13424.80
3498.51
0.11
0.01
0.04
0.03
3483
11293.6
186379
22750
5851848
93.78
32.70
38.96
17.52
47.22
36.11
102.76
0.001
50044
79683
4368
1572
580.69
9.4
89.13
63.19
96.89
93.07
110.96
55.03
32.97
35.06
42.99
593.47
432.62
328.08
269.70
535.78
313.09
1659
278.44
205.52
191.79
152.30
14.83
3.11
0.19
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.00
0.05
0.82
0.66
0.58
0.69
0.68
0.71
0.54
0.41
0.43
0.48
0.95
0.93
0.92
0.90
0.94
0.91
0.97
0.93
0.61
0.60
0.44
0.27
0.05
–
Note. DF: degree of freedom; SS: sum of squares; SST: sum of squares total; F: Fisher test; P: <0.05-significant differences; R2: explanatory percentage; RGRh: relative
growth in height, RGRd: relative growth in diameter; RGRll: relative growth in leaf length; RGRlw: relative growth in leaf width; TLP: total leaf production; TLA: total
leaf area.
(Fig. 2A). The synchronism of leaf senescence and abscission was low,
but foliar budding was high in all three treatments. Only in T25, from
the 17th week there was a suspension of budding in 44% of the moni­
tored plants. In the peak period of leaf senescence, the percentage of
plants that exhibited such phenophases were 23.33% (T100), 43.35%
(T50), and 56.66% (T25). At the peak period of foliar abscission, the
percentages were 13.3% (T100), 26.6% (T50), and 30% (T25) (Fig. 3a).
Flowering phenological rhythm (F ¼ 41.66, p < 0.05), fruiting (F ¼
Fig. 3. Circular graphs evidencing the effect of simulated reduction of soil water availability on the (a) vegetative and (b) reproductive phenological rhythm of
Talinum paniculatum (Jacq.) Gaertn. T: treatments; T100: 100% FC, T50: 50% FC, T25: 25% FC; FC ¼ field capacity. Bars around the circle refer to the weekly or daily
percentages of phenological activity for each treatment. The direction of the arrows indicates the mean date or mean angle (μ) and the length of the arrows indicates
the degree of seasonality (r) in each treatment.
5
B.A.S. Aguiar et al.
Acta Oecologica 107 (2020) 103617
growth, the primary responses to abiotic stress are concentrated in these
traits. In general, plants respond to water deficit with lower heights,
reductions in length, width and leaf area, resulting in lower accumula­
tion of biomass (Chaves et al., 2002, Osakabe et al., 2014), which was
also recorded in T. paniculatum. However, plants height remained con­
stant between T100 and T50, which shows an adjustment to the
reduction of 50% of water in the soil.
The reductions in leaf area recorded in herbs from semi-arid envi­
ronments (Lu et al., 2011; Yousfi et al., 2015), despite reducing the
photosynthetic rates, are signaled as a strategy to minimize transpira­
tion, aiming at saving water (Lambrecht et al., 2017). In addition, spe­
cies adapted to drought invest in increasing leaf thickness to compensate
for the negative effect of leaf area reduction on photosynthesis, as they
would have the advantage of the better light interception, and therefore
a higher carbon gain (Chaves et al., 2002). However, the water deficit
effect on the number of leaves produced is not always detected, but they
are able to maintain production (Wang et al., 2009) or increase it as
occurred in this study in the T50, under moderate water reduction
condition. It is important to emphasize that the increase in leaf pro­
duction in T50 can represent a strategy to increase energy and water
reserves in the tissues, that later will be translocated for reproduction or
survival of the plants.
From a physiological point of view, in response to water deficit,
plants may reduce stomatal opening generating limits on CO2 absorption
and photosynthetic activity (Chaves et al., 2002; Pe~
nuelas et al., 2004;
Martı ̀nez et al., 2004; Moreno et al., 2008; Xu et al., 2010, Osakabe et al.,
2014; Correia et al., 2016), and may increase the level of abscisic acid
(ABA) (Golldack et al., 2014) and of ethylene (Chaves et al., 2003) in
their tissues, with direct implications in their growth. Although such
responses were not evaluated in this study, reductions in the vegetative
growth of T. paniculatum may also be reflecting the changes in their
photosynthetic activity and in their hormonal levels.
Only in T25, it was observed significant reductions in height growth,
besides inhibiting leaf sprouting, increasing senescence, and antici­
pating and intensifying leaf abscission. These responses occurred in the
third month of plant life, and indicate that variations in the vegetative
phenological rhythm are secondary responses observed in prolonged dry
conditions. Thus, we suggest that premature senescence of leaves in
prolonged drought conditions can affect the efficiency of species carbon
~ uelas, 2015).
capture and the ecosystem nutrient cycle (Estiarte and Pen
It should be mentioned that future climate scenarios may induce greater
overlap between insect and herbaceous phenological activity, leading to
pest outbreaks and massive losses in plant production (Morellato et al.,
2016).
Table 2
Circular analysis of vegetative and reproductive phenological patterns of Tali­
num paniculatum (Jacq.) Gaertn. under reduced soil water availability.
Phenophases
Variable
T100
T50
T25
Foliar budding
Observations
Mean angle (μ)
Circular standard
deviation
Length of mean vector (r)
Observations
Mean angle (μ)
Circular standard
deviation
Length of mean vector (r)
Observations
Mean angle (μ)
Circular standard
deviation
Length of mean vector (r)
Observations
Mean angle (μ)
Circular standard
deviation
Length of mean vector (r)
Observations
Mean angle (μ)
Circular standard
deviation
Length of mean vector (r)
Observations
2500
349�
174.3�
2500
349�
174.3�
2157
203.7�
121.6�
0.01
111
306.5� *
39.3�
0.01
145
313� *
40.4�
0.1
333
302.2� *
37.4�
0.79
61
319.8� *
25.5�
0.77
77
322.3� *
24.8�
0.8
87
321.3� *
26�
0.9
4166
289.7� *
48.2�
0.91
1880
307.5� *
39.3�
0.9
**
**
**
0.7
5060
298� *
43.4�
0.79
1873
309.7� *
35.2�
**
**
**
**
0.75
2653
0.82
1020
**
**
Mean angle (μ)
Circular standard
deviation
Length of mean vector (r)
315� *
32.3�
324.9� *
23.4�
**
**
0.85
0.92
**
Foliar senescence
Foliar abscission
Flowering
Fruiting
Dehiscence of
fruits
Treatments
Note. T: treatments, T100: 100% field capacity (FC), T50: 50% FC, T25: 25% FC;
*Significant mean angles (μ) by Rayleigh test (P < 0.05); **No data (absence of
reproduction).
8.26, p ¼ 0.004), and fruit dehiscence (F ¼ 3.717, p ¼ 0.04) differed
among treatments (Fig. 3b). Flowering synchrony was high (83.3%) in
the control and decreased to 56.6% in T50, with a temporal delay of 19
days. The fruiting synchrony was high (100%) at the control and low
(53.3%) at T50, with a delay of 21 days. The fruit dehiscence had high
synchrony in the control (83.3%), but decreased to 36.6% in T50, with a
temporal delay equal to fruiting (Fig. 3b). Seed viability was similar
between treatments, with 68.3% germination in the control and 66.6%
in T50. GLM analysis showed that about 5%–61% of phenological
rhythm was explained by the reduction of soil water availability
(Table 1).
4.2. Reproductive responses
The reduction of soil water availability negatively affects the
reproduction of T. paniculatum. A 50% reduction in water caused a delay
in reproductive phenology and reduction in morphometry and produc­
tion of flowers, fruits, and seeds of T. paniculatum. These reductions were
drastic when we applied a 75% reduction in water supply, and there was
a complete absence of flower and fruit production, as already registered
for some herbaceous and sub-shrub species (Sharp et al., 2009; Crim­
mins et al., 2010; Su et al., 2013; Yousfi et al., 2015).
In general, changes in the amount and seasonal distribution of
rainfall have, either isolated or combined, negative effects on flowering,
fruiting, and seed production of bush and herbaceous plants in field
conditions (Morellato et al., 2013; Zeppel et al., 2014), affecting pro­
cesses of recruitment and renewal of plant populations from semi-arid
~ uelas et al., 2004). Under laboratory conditions, re­
environments (Pen
ductions in water supply also have negative effects on plant flowering,
fruiting, and seed production (Cacho et al., 2013; Miranda et al., 2014;
Yousfi et al., 2015).
According to this study, negative effects of water supply reduction
would be expected on the viability of the seeds formed. However, in
4. Discussion
4.1. Vegetative responses
The reduction in soil water availability negatively influenced the
vegetative growth of T. paniculatum. The treatment that simulated
greater water deficit caused drastic reductions in all herb attributes.
These reductions were partially expected in the vegetative responses
because, in most plants, water deficit induces changes in the pheno­
logical vegetative behavior and generates reductions in tissues growth
~ uelas et al., 2004; Miranda et al., 2009; Muller
that are expanding (Pen
et al., 2011), affecting plant productivity (Gibson-Forty et al., 2016).
However, we expected the facultative CAM photosynthetic pathway
adopted by this species, reported in previous studies, to have an opti­
mized relationship in carbon fixation mode and water loss (Guerere
et al., 1996; Assaha et al., 2017), which was observed only in T50.
The study showed that plant diameter and foliar morphometry
respond rapidly to water deficit, suggesting that, during the vegetative
6
B.A.S. Aguiar et al.
Acta Oecologica 107 (2020) 103617
spite of the significant differences in T. paniculatum fruit and seed pro­
duction between the control and T50 treatments, plants produced seeds
with high viability, indicating that in the natural environment, forest
regeneration will be affected by the reduction in seed production, but
not by seed viability. In contrast, responses may diverge in species
reproduction, increasing flowers production under arid conditions to
ensure significant seed production (Xie et al., 2016). However, it is
necessary to consider the weight and size of the fruits, which were
smaller in the study, as well as the size and weight of the seeds, since
reductions in these structures lead to lower metabolic reserves, affecting
seedlings performance, which reduce their establishment and survival
(Benard and Toft, 2007).
The phenological flowering rhythm in water-deficient situations or
in forest soils that are more exposed to direct light can be anticipated
(Sharp et al., 2009; Souza et al., 2014; Kazan and Lyons, 2016; Takeno,
2016), delayed (Prieto et al., 2008; Crimmins et al., 2010; Su et al.,
2013), or suffer inhibition (Yousfi et al., 2015), showing that herbaceous
response may diverge. In this study, T. paniculatum presented delay and
shorter flowering time and also short anthesis in response to water
deficiency. These findings, coupled with reductions in the size of floral
structures and changes in flower color, suggest that rainfall irregularity
in semi-arid forests, as predicted by climate changes, may influence the
plant attractive power to their pollinators, due to the reduction of floral
display (Su et al., 2013; Lambrecht et al., 2017). This fact could lead to
even greater reductions in seed production, considering compulsory
cross-breeding species, which also present negative effects for some
animal populations that assist in the dispersal process (Stenseth and
Mysterud, 2002; Saavedra et al., 2003).
In general, herb responses were not proportional to the water supply
reduction, i.e. reducing soil water availability by 50% and 75% may
induce greater reductions in the size and production of plant vegetative
and reproductive structures, as well as the time when phenophases start.
This finding leads us to question whether such reductions will also occur
when water restrictions increase in forest soils in dry environments due
to interannual variations in the total amount and rainfall distribution
(Araújo et al., 2007; Bernal et al., 2011; Asbjornsen et al., 2011; Albu­
querque et al., 2012; Miranda et al., 2014; Becerra, 2014; Knapp et al.,
2018), especially when rainfall is stochastic in the Caatinga vegetation
and can influence the number of individuals in the populations (Reis
et al., 2006), the occurrence and distribution of the species (Araújo et al.,
2005), and population renewal (Silva et al., 2015).
Undoubtedly, in field conditions, it is difficult to estimate the per­
centage of water reduction that induces changes in plant growth and
reproduction because other soil physical-chemical variables may
interact with water, making the plant response speed of plants faster or
slower (Araújo et al., 2005; Holmgren et al., 2012; Richardson et al.,
2013; Silva et al., 2016). Taking these difficulties into account, many
studies simulate water constraints (Miranda et al., 2014; Yousfi et al.,
2015), because such experiences reflect reality and provide a broad view
of how ecosystems will respond to future climate changes (Knapp et al.
al., 2018).
Considering the prediction of rainfall reduction of 30%–70% in dry
tropical forests (Dai, 2013; Vicente-Serrano et al., 2013; PBMC et al.,
2014; IPCC, 2014), data from this study show that the consequences of
soil water restrictions of the Caatinga vegetation can generate signifi­
cant damages to the cover of the studied species, as well as to those with
similar strategies. Based on the founded evidence, phenological imbal­
ances will reflect on their reproductive success, since they lead to
asynchrony with the life cycle of animals that actively participate in
pollination and dispersal processes (Morellato et al., 2016). In addition,
it is probable that reductions will occur in plant seed production that
annually renews the soil bank stock of the forests, mainly if we consider
that 32%–67% of the soil seed bank density is explained by the inter­
annual rainfall variation (Silva et al., 2015).
The explanations of the pulsed herbaceous occurrence, (Araújo et al.,
2005), or the existence of a reduction in the size of their populations
(Reis et al., 2006), may be related to the low water availability in the soil
due to the prolonged droughts in consecutive years in these forests.
However, this evidence needs to be better investigated in studies that
simulate the effect of rainfall on herbaceous species communities.
5. Conclusion
We suggest that increasing soil water supply constraints may be
negative for T. paniculatum, causing limitations and delay in its growth
and reproduction. This effect is more drastic with a prolonged 75%
reduction in soil water availability, which inhibits its reproductive
processes. In addition, we do not rule out that the reductions in attri­
butes can be considered as water-saving strategies. However, the pre­
dicted effect of reducing rainfall in dry tropical forests will likely
compromise the reproductive success and population growth of a species
that is considered drought-tolerant.
Author contributions
AMMS, KAS, JTS and ELA formulated the idea and contributed to the
literature review. BASA, ESSS and VKRA built the experiment and
collected the data. BASA, KAS and AMMS performed the statistical
analysis. ELA, JMFFS and DMS reviewed the work and contributed to
the discussion of the results. BASA wrote the article with collaboration
from all co-authors.
Declaration of competing interest
None.
Acknowledgments
~o de Amparo a Ci^encia e Tecno­
We thank FACEPE/Brazil (Fundaça
logia do Estado de Pernambuco; process APQ-0083-2.05/15), which
funded and supported the construction of the experiment. To CNPq/
�gico;
Brazil (Conselho Nacional de Desenvolvimento Científico e Tecnolo
process 131700/2015-4) who provided the author’s scholarship. We
^mico de Pernambuco) and the
thank the IPA/Brazil (Instituto Agrono
UFRPE/Brazil for their logistical support. We thank all the researchers at
the Natural Ecosystems Plant Ecology Laboratory (LEVEN) for their
assistance in collecting and analyzing the data.
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Contribuiç~
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