Acta Physiologiae Plantarum (2023) 45:41

https://doi.org/10.1007/s11738-023-03525-8

ORIGINAL ARTICLE

The ecophysiological responses of Copernicia prunifera palm trees

to soil constraints and competition with invasive Cryptostegia
madagascariensis in tropical dryland
Wiliana Júlia Ferreira de Medeiros1 · Claudivan Feitosa de Lacerda2 · Roberta Boscaini Zandavalli3 ·
Isabel Cristina da Silva Araújo2 · Carlos Henrique Carvalho de Sousa4 · Antonio Marcos Esmeraldo Bezerra5 ·
Aureliano de Albuquerque Ribeiro2 · Régis dos Santos Braz1

Received: 16 October 2021 / Revised: 27 November 2022 / Accepted: 30 January 2023

© The Author(s) under exclusive licence to Franciszek Górski Institute of Plant Physiology, Polish Academy of Sciences, Kraków 2023

Abstract
Biological invasions have modified the terrestrial biota worldwide, reducing biodiversity, and causing economic loss. Coper-
nicia prunifera (Carnauba), a palm tree native to the semi-arid region of Brazil (Caatinga ecosystem), has high economic
and social importance, but has been impacted by the invasive climbing shrub Cryptostegia madagascariensis (Madagascar
rubber vine). We evaluated physiological, biochemical, and nutritional responses in mature plants of both species in two
locations: Catuana (where there is an intense water-deficit during the dry season) and Minguaú (where there is high salinity
and sodicity, and excess water throughout the year). Our results show that competitive interaction between the two species is
mainly defined by their adaptability to abiotic soil constraints. C. prunifera is better adapted to severe water-deficit conditions,
but its ecophysiological performance is not sufficient to withstand invasion by C. madagascariensis. The invader is more
competitive in flooded, salt-affected soils, and is not severely impacted even with high sodium accumulation in its leaves.
Our results also show that the negative impacts on C. prunifera intensify at the final stage of infestation, when the shading
caused by C. madagascariensis restricts access to solar radiation and accelerates leaf senescence. However, the impact on
C. prunifera precedes the permanent shading, as evidenced by the inhibition of net assimilation of C ­ O2 under intermediate
levels of infestation. These results reinforce the vulnerability of carnauba populations in the Caatinga ecosystem, which may
be severely impacted without the development of technologies to mitigate the impact of invasion.

Keywords Caatinga · Carnauba forest · Invasive species · Drought stress · Waterlogging · Salt-affected soils

Introduction

Biological invasions have modified the terrestrial biota

worldwide, causing changes in the functionality of native
Communicated by F. Araniti. species in communities, altering evolutionary processes
and reducing biodiversity (Reimánek and Richardson 1996;
* Claudivan Feitosa de Lacerda
Grice 2008; Schnitzer and Carson 2010; Martínez-Izquierdo
cfeitosa@ufc.br
2016; Silva et al. 2017; Linders et al. 2019). In general, plant
1
Department of Soil Science, Federal University of Ceará, species become invasive because they have some attributes
Fortaleza, Ceará, Brazil that make them better competitors than native species, such
2
Department of Agricultural Engineering, Federal University as rapid growth, numerous and easily dispersed seeds, a high
of Ceará, Fortaleza, Ceará, Brazil germination rate, and production of allelopathic substances
3
Department of Biology, Federal University of Ceará, (Reimánek and Richardson 1996; Silva et al. 2017).
Fortaleza, Ceará, Brazil In addition to the characteristics of the invasive spe-
4
Faculdade Ieducare -FIED, Tianguá, Ceará, Brazil cies, invasibility depends on environmental stresses and
5
Department of Agronomy, Federal University of Ceará, resource availability (Lonsdale 1999). It has been postu-
Fortaleza, Ceará, Brazil lated that the success of invasion is positively related to

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resource availability, i.e., as resources become increas-
ingly available, the habitat becomes increasingly invasible
(Davis et al. 2000). This hypothesis has been supported by
previous works with herb species in a garden experiment
(Agrawal et al. 2005) and with grasses in a field experiment
(Going et al. 2009). However, there was no direct relation-
ship between nutrient availability and invasion success in a
pot mesocosms experiment with six levels of nutrient supply
(Liu et al. 2018).
Another less-explored relationship exists between envi-
ronmental stress and invasibility. High levels of abiotic con-
straints reduce the chances of invader success (Alpert et al.
2000), as shown in a desert field experiment, where severe
water shortage prevented annual non-native spread in the
drought treatment (Suazo et al. 2012). Otherwise, invasive
species with fast growth ability can be favored in situations
where water shortages cause mortality in the native spe-
cies (Manea et al. 2016; Mojzes et al 2020). The ability
to tolerate stressful and resource-limited conditions is part
of the strategy that renders an invasive species capable of
invading a wide range of environments, i.e., high pheno-
typic plasticity (Richardson and Pys̆ek 2006). Although the
relationship between abiotic stress and invasibility has been
studied, there is no consensus, and therefore, more studies
need to be carried out.
In this study, we investigated the effect of resource avail-
ability and environmental stress on an invasive climbing
shrub (Madagascar rubber vine) and its native palm support
plant (carnauba) at different levels of infestation. Mada-
gascar rubber vine [Cryptostegia madagascariensis Bojer
ex Decne, Apocynaceae], a shrub with climbing branches
(Flora do Brasil 2020), occurs in almost all continents
(Judd et al. 2009). In regions of Australia, the United States,
Kenya, Hawaii, India, Virgin Islands, Saint Lucia, Mont-
serrat, Anguilla, Puerto Rico and Brazil (Invasive Species
Specialist Group 2010), this species has become an invasive
plant, causing environmental and economic damage. Mada-
gascar rubber vine is a climbing shrub, heliophyte, occurring
from the coast to drier regions such as savannas in Brazil,
notably dominating disturbed zones and areas of riparian
and seasonally flooded forests (Endress and Bruyns 2000;
Klackenberg 2001; Flora Brasil 2020). It is an endemic
species of the Islands of Madagascar and has changed the
floristic composition and structure of plant communities in
many ecosystems around the world (Lowe and Walker 1977;
Whigham 1984; Judd et al. 2009; Sousa et al. 2016; Bar-
bosa et al. 2019). As a climbing shrub (Flora Brasil, 2020)
about 2.0 to 3.0 m tall, C. madagascariensis develops over
the canopy of native trees (up to 15 m in height), killing
them by preventing the passage of light and causing exces-
sive shading (Andrade 2013; Cruz et al. 2016; Sousa et al.
2016). C. madagascariensis, thrives in open environments,
its root system growing around the host’s rhizosphere and
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Acta Physiologiae Plantarum (2023) 45:41
competing for soil resources (Dillenburg et al. 1995; Toledo-
Aceves and Swaine 2008).
In Brazil, the Madagascar rubber vine was introduced
for ornamental purposes but became an invader in areas
occupied by Carnauba [Copernicia prunifera (Miller) H. E.
Moore, Arecaceae] (Sousa et al. 2015; Flora do Brasil 2020).
C. prunifera is a palm tree native to the Caatinga ecosystem,
a large (850,000 ­km2) geographical area in northeastern Bra-
zil, comprising different vegetation types under a dry tropi-
cal climate (Miles et al. 2006; Santos et al. 2014; Campos
et al. 2020). This palm tree reaches a height of 10 to 15 m,
stem diameter of 15 to 25 cm, and botanical maturity (first
flowering) between 12 and 15 years old. Carnauba stands
out for its economic and social importance, especially for
the wide variety of products obtained from its extractive
exploitation, such as the wax that covers its leaves (the most
important product), building materials, crafts, and animal
feed (Pereira et al. 2014; Sousa et al. 2015; Garcez et al.
2020). In Brazil, 905 tons of wax (BRL 15.6 million gross
income) and 19,465 tons of powder (BRL 219.1 million
gross income) were produced in 2019. However, these natu-
ral landscapes have been modified by anthropic activities,
either by deforestation to implement agricultural enterprises
(Sousa et al. 2015) or by the introduction of invasive species,
causing social and economic consequences.
Most carnauba populations are located in the river valleys
of the Caatinga, in areas of Alfisols and Entisols. During
the rainy season, parts of these areas become extensively
flooded (Moro et al. 2015), and soils are prone to salinity
and sodicity problems. However, during the prolonged dry
season (6 to 8 months), plants are subjected to severe water
deficits, especially in non-flooded areas. By tolerating these
different environmental restrictions, C. prunifera demon-
strates high plasticity, explained, at least in part, by traits that
reduce water loss, including wax accumulation on leaf sur-
faces, and a porous root system which favors survival under
conditions of temporary anoxia. Despite its high plasticity,
the threat of C. madagascariensis to carnauba populations in
the Caatinga ecosystem has become quite evident in recent
years, with the death of hundreds of carnaubas in various
stages of development caused by complete shading (Cruz
et al. 2016; Sousa et al. 2016).
To understand the degree of vulnerability of different
kinds of environment dominated by carnauba, we investigate
whether the native or invasive species has greater plasticity
to withstand the environmental constraints of the Caatinga
ecosystem. In fact, almost nothing is known about how envi-
ronmental factors, such as soil moisture and soil salinity,
affect the ecophysiological responses of C. prunifera and C.
madagascariensis during this interspecific competition. We
expect C. madagascariensis to maintain leaf gas exchange
rate and competition capacity with C. prunifera in environ-
ments with different edaphic conditions. The aim of this
 Acta Physiologiae Plantarum

Table 1  Chemical characterization of the soils in the Catuana and Minguaú experimental areas, in the 0–20 and 0–40 cm layers
Experimental pH Ca2+ Mg2+ Na+ K+ H+ + ­Al3+ Al3+ ECe
(2023) 45:41

areas (H2O) (cmolc ­kg−1) (dS ­m−1)

Catuana (0–20 cm) 4.5 2.3 1.7 0.10 0.44 4.5 1.0 0.14
Catuana (0–40 cm) 4.5 2.5 2.6 0.11 0.39 4.3 1.3 0.14
Minguaú 4.4 1.9 1.9 1.60 0.08 2.6 0.2 3.47
(0–20 cm)
Minguaú 4.5 1.9 2.7 1.69 0.09 1.8 0.3 3.50
(0–40 cm)
S T V ESP P SOM C N C/N
(cmolc ­kg−1) (%) (%) (mg ­kg−1) (g ­kg−1)

Catuana 4.5 9.0 50 1 6 10.9 6.3 0.7 9

(0–20 cm)
Catuana 5.6 9,9 57 1 6 9.8 5.7 0.6 9
(0–40 cm)
Minguaú 5.5 8.1 67 20 9 10.8 6.3 0.7 9
(0–20 cm)
Minguaú 6.4 8.2 78 21 7 5.9 3.4 04 10
(0–40 cm)

ECe electrical conductivity of the saturation extract, S sum of exchangeable bases, T cation exchange capacity, V base saturation, ESP exchangeable sodium percentage, SOM soil organic matter
Page 3 of 18
41

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Fig. 1  Monthly rainfall (a) and soil moisture (b) in two experimen-
tal areas, during the rainy and dry season of 2016 and 2017. Arrows
indicate the sampling time for soil and plant materials
study was to better understand the competitive interaction
between C. prunifera and C. madagascariensis, and how
each species withstands the soil abiotic constraints present
in tropical dryland conditions. To this end, we evaluated
the physiological, biochemical, and nutritional responses of
mature C. prunifera and C. madagascariensis in two car-
nauba populations representative of the Caatinga ecosystem
in both a flooded and non-flooded location in the dry and
rainy seasons.
Material and methods
Location and characterization of the study locations
The study was conducted between 2016 and 2017 in two
distinct locations: Catuana (03°41.625’S; 38°53.028W;
50 m), and Minguaú (03°49.152’S; 38°44.434W; 20 m),
both in the municipality of Caucaia, Ceará, Brazil (Sup-
plementary material S1). The distance between the two
areas is approximately 23 km, and the climatic condi-
tions are similar. In both locations, the mean monthly
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Acta Physiologiae Plantarum (2023) 45:41
air temperature varies from 26.2 to 27.3 °C and poten-
tial annual evapotranspiration is higher than 1700 mm.
The mean annual rainfall is 970.0 mm for Catuana and
1061.4 mm for Minguaú, with about 80% of rainfall
occurring in the rainy season (February to May).
Characterization of soil abiotic constraints
The areas of Catuana and Minguaú were chosen because of
the presence of carnauba populations infested by C. mada-
gascariensis, and because they have different intensities of
abiotic constraints, related to the edaphic and topographic
conditions. The soils were classified as Haplic Planosol
(Alfisol) and Natric Planosol (Alfisol), in Catuana and Min-
guaú, respectively. These soils are usually located in areas
of flat or gently undulating relief and show a high accumula-
tion of clay in the subsurface horizon (Jacomine et al. 1973;
EMBRAPA 2018), factors that favor flooding, especially
during the rainy season.
Minguaú is located at the lower part of the terrain, near a
lagoon, and is favorable to flooding during the rainy season.
The soil type (Natric Planosol) in Minguaú has high salinity
and sodicity, as confirmed by previous soil analyses per-
formed at depths of 0–20 and 20–40 cm (Table 1). Catuana
is located at the highest part of the terrain and has a slight
slope, factors that reduce flooding during the rainy season
but intensify the water-deficit in the dry season. This area
does not have high salinity and∕or sodicity (Table 1). Elec-
trical conductivity of soil saturation extract (ECe; Richards
1954) data obtained at 0–20 cm depth, during the dry and
rainy seasons (2016/2017), confirms the higher salinity in
the Minguaú area, with a 32% increase between the rainy
(3.29 ± 0.02 dS ­m−1) and dry periods (5.11 ± 0.64 dS m ­ −1).
In Catuana, the ECe values were 0.14 ± 0.00 and 0.49 ± 0.02
dS ­m−1, for the rainy and dry seasons, respectively.
Monthly rainfall data (Fig. 1a) and changes in soil mois-
ture were also evaluated for two years (2016 and 2017) in
both areas. Soil samples were collected in April (rainy sea-
son) and October (dry season), at 0–20 cm depth and about
50 cm away from the stem of C. prunifera and C. madagas-
cariensis (15 plants of each species at each sampling event),
and soil moisture was obtained by the thermogravimetric
method (EMBRAPA 2017). Soil moisture values were high
in Minguaú, which was flooded throughout the rainy season
and had relatively high soil moisture even during the dry
season (Fig. 1b). In relative terms, soil moisture in the dry
season was 73.3% and 35.9% lower than in the rainy season,
in the Catuana and Minguaú areas, respectively.
Acta Physiologiae Plantarum (2023) 45:41
Fig. 2  a Infestation levels of C. madagascariensis on C. prunifera.
1—C. prunifera without infestation; 2—C. madagascariensis starting
to grow on the carnauba stem; 3—C. madagascariensis reaching the
whole stem of the carnauba, but without covering the leaves; 4—C.
Sample design and relative infestation
Five levels of C. madagascariensis infestation of C. prunif-
era were defined, considering the growth of the invasive
species over the whole native plant: 1. C. prunifera without
infestation; 2. C. madagascariensis plant starting to grow on
the carnauba stem; 3. C. madagascariensis plant spanning
the whole carnauba stem, but without covering the leaves;
4. C. madagascariensis plant covering part of the carnauba
leaves; and 5. C. madagascariensis plant fully covering the
carnauba canopy (Fig. 2a).
The relative infestation (RI) was estimated in an area of
1.0 hectare for both Catuana and Minguaú. The values of RI
were obtained by relating the number of mature C. prunifera
plants at each level of C. madagascariensis infestation (1–5)
to the total number of mature C. prunifera plants in an area
of 1.0 hectare. The weighted mean of the relative infestation
for each area was then calculated, according to the equation
described below:
∑5
RI = (npxLi)∕NT
Li=1
Page 5 of 18 41
madagascariensis covering part of the carnauba leaves; and 5—C.
madagascariensis fully covering the carnauba canopy; b Percentage
of C. prunifera plants infested by the invasive species for each previ-
ously defined level of infestation, in the two experimental areas
where, RI = relative infestation; np = number of plants of C.
prunifera per hectare for each level of infestation; Li = level
of infestation (1 to 5); NT = total number of C. prunifera
plants per hectare.
The percentage of C. prunifera plants infested by C. mad-
agascariensis plants varied between the areas and with the
pre-established attack level (Fig. 2b). In Catuana, approxi-
mately 67% of the plants had no infestation or infestation
was just starting, whereas in Minguaú, approximately 55%
of the carnauba palm trees were either almost or completely
covered. The average relative infestation was 29.3% in Catu-
ana and 52.1% in Minguaú.
In both locations (Catuana and Minguaú), five mature
C. prunifera plants were selected, at each level of infesta-
tion, and were evaluated in April (rainy season) and October
(dry season) over two years (2016 and 2017). The mean
plant height and the stem diameter for the selected plants
were: 9.1 ± 0.4 m, 23.0 ± 0.6 cm (Catuana) and 8.9 ± 0.6 m,
21.5 ± 1.5 cm (Minguaú) respectively. A repeated measures
design was implemented in the arrangement of split plot,
with two areas (Catuana and Minguaú), five levels of infes-
tation (1 to 5) and two sampling seasons (rainy and dry).
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 41 Page 6 of 18
Plant measurements
All physiological, biochemical, and nutritional analyses
were performed on leaves of mature C. prunifera and C.
madagascariensis plants. The methods for sampling and
analysis are described below.
Leaf gas exchange
Leaf gas exchange evaluations were performed in five plants
of C. prunifera and C. madagascariensis, in fully expanded
mature leaves (one leaf per plant), using a portable infrared
gas analyzer (LI-6400XT, Li-Cor, USA). For C. prunifera,
the leaves were excised and measurements were taken imme-
diately. For C. madagascariensis, the measurements were
performed with the leaves attached to the plants, in both
the rainy and dry season (remaining leaves). All measure-
ments were performed in the morning, between 8:00 and
11:00 h, using an artificial radiation source with an intensity
of 1600 μmol ­m−2 ­s−1, air flow rate of 500 µmol ­s−1, and
under environmental conditions of air temperature, relative
humidity and C ­ O2 concentration (about 390 µmol m ­ o1−1).
During all measurements, leaf temperature ranged from 29.9
to 36.2 °C (C. prunifera) and from 29.7 to 35.7 °C (C. mada-
gascariensis). These variations for the relative humidity in
leaf chamber were from 45.4 to 57.9% (C. prunifera) and
from 42.8 to 59.6% (C. madagascariensis). The stabiliza-
tion time for each measurement of leaf gas exchange ranged
from 1.5 to 2.0 min.
Organic solutes
After reading the gas exchange, the middle third of the
leaves of C. prunifera and C. madagascariensis was col-
lected. The leaves were removed, wrapped in aluminum foil,
and immediately placed in liquid nitrogen. The samples were
then stored in a freezer (− 20 ºC) and subsequently subjected
to the freeze-drying process. The freeze-dried material of
C. prunifera was crushed in a Wiley-type mill (model MA
340, Marconi, Brazil) and that of C. madagascariensis was
macerated in liquid nitrogen. The extracts for the determina-
tion of organic solutes were obtained according to Cataldo
et al. (1975). Soluble carbohydrate determination was based
on the phenolsulfuric acid method followed by absorbance
readings at 490 nm, using as standard D-glucose reagent
(Dubois et al. 1956). Soluble N-amino concentration was
measured using the ninhydrin method performed by Yemm
and Cocking (1955), followed by absorbance readings at
570 nm using glycine as standard. Proline was quantified
following the ninhydrin method and by reading the absorb-
ance at 520 nm, using proline as standard (Bates et al. 1973).
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Acta Physiologiae Plantarum (2023) 45:41
The readings were performed in a spectrophotometer (model
UV-1650PC, Shimadzu, Japan).
Nutritional status of plants
The nutritional status of the plants was evaluated with the
same freeze-dried and crushed plant material used to deter-
mine organic solutes. To determine the leaf concentrations
of calcium, magnesium, phosphorus, iron, zinc, copper and
manganese, the plant material was subjected to wet diges-
tion with nitric and perchloric acid (­ HNO3 + ­HClO4) in the
proportion of 3:1 (EMBRAPA 2017). The analyses of Ca,
Mg, Fe, Zn, Cu, and Mn were performed by atomic absorp-
tion spectrophotometry. Phosphorus was determined accord-
ing to a colorimetric method, reading the absorbance at
660 nm (EMBRAPA 2017). Nitrogen concentrations were
obtained by extraction with sulfuric digestion and determi-
nation by the Kjeldahl method, adapted from Bremner and
Mulvaney (1982) and Tedesco (1995). The extracts used
to chloride, sodium, and potassium were obtained accord-
ing to the methodology proposed by Cataldo et al. (1975).
Chloride concentration was determined spectrophotomet-
rically (reading the absorbance at 460 nm) following the
Hg(SCN)2—Fe(NO3)3 method described by Gaines et al.
(1984). Phosphorus and chloride readings were performed in
spectrophotometer (model UV-1650PC, Shimadzu, Japan).
Sodium and potassium concentrations were determined by
flame photometry.
Statistical analysis
ANOVA was performed using the statistical program SIS-
VAR v.5.5 (Ferreira 2010), using the split plot model. Data
were subjected to the Shapiro–Wilk normality test as a pre-
requisite for the analysis of variance by the F test, and when
denoted significant, a t test was performed (5% probability).
The data were subjected to multivariate analysis of vari-
ance (MANOVA) and integrated by performing Pearson’s
correlation matrix analysis, principal component analysis
(PCA) and hierarchical clustering, with the statistical pro-
gram SPSS v.16. Kaiser–Meyer–Olkin (KMO) and Bartlett’s
sphericity tests were used to evaluate the adequacy of the
sample. All statistical analyses were performed using the
mean of the two years of evaluation (2016 and 2017) for
each season (dry and rainy), with three repetitions.
Results
Pearson’s correlation, PCA and cluster analysis
The three-way analysis of variance (Table 2) showed sig-
nificant effects for the three-way interaction (infestation
 Acta Physiologiae Plantarum

Table 2  Three-way analysis of variance (F values) of the effects of infestation levels (IL), areas (A) and season (S) on leaf gas exchange, organic solutes contents and mineral nutrition of C.
prunifera and C. madagascariensis
F Values
(2023) 45:41

A gs Ci E Pro Carb N-amino N P K Ca Mg Na Na/K Cl Fe Cu Zn Mn

Copernicia prunifera
IL 144.0** 83.5** 7.3** 76.8** 2.7 ns 8.4** 267.4** 232.8** 7.8** 28.1** 39.7** 3.7 ns 15.2** 82.4** 6.3* 32.3** 1.9 ns 74.6** 22.3**
A 8.3* 8.6* 114.4** 27.0** 36.5** 147.3** 43.8** 1.11 ns 4.7 ns 224.1** 0.43 ns 23.8** 1213** 1738** 524.0** 396.2** 1.0 ns 8.5* 10.1**
S 497.3** 200.8** 4.1 ns 137.0** 12.0** 85.3** 61.4** 0.0 ns 0.1 ns 33.8** 38.5** 4.8* 583.7** 353.0** 146.8** 593.6** 4.9* 1.9 ns 43.4**
ns ns ns ns
IL x A 16.1** 2.4 4.0* 0.1 3.6* 9.1** 5.3* 5.7* 18.1** 10.2** 1.0 1.6 8.8** 31.5** 6.5** 6.5** 6.5** 62.3** 5.9*
IL x S 3.6* 9.5** 4.4** 14.7** 6.8** 3.0* 7.7** 3.7* 1.0 ns 13.2** 12.3** 0.9 ns 19.4** 14.7** 18.4** 4.9** 3.5* 17.4** 13.5**
AxS 100.5** 105.4** 17.0** 98.0** 51.0** 52.8** 29.1** 9.5** 36.7** 117.4** 0.9 ns 4.6* 586.6** 396.1** 70.7** 362.3** 0.0 ns 21.7** 115.3**
ns ns
IL x A x S 10.6** 2.1 1.9 0.9* 3.3** 3.23* 4.7** 4.7** 4.5** 6.0** 31.4** 4.4* 26.5** 18.3** 4.2* 31.7** 3.7* 8.7** 41.4**
Cryptostegia. Madagascariensis
IL 19.8** 4.7* 0.3 ns 6.2** 22.5** 16.8** 1.4 ns 13.4** 3.1 ns 20.2** 25.4** 3.7 ns 23.8** 33.1** 31.9** 20.5** 2.5 ns 22.3** 1.1 ns
ns ns ns ns ns ns ns
A 789.5** 2.8 1.9 30.9** 9.1* 113.1** 0.1 246.3** 141.1** 1.6 48.3** 4.2 3439** 1716** 49.1** 0.0 4.9 11.0** 7.1*
S 1462** 848.3** 16.8** 852.5** 13.9** 0.1 ns 9.1** 44.0** 83.2** 1129** 125.3** 43.5** 513.4** 1692** 129.2** 3.3 ns 42.7** 0.7 ns 16.1**
IL x A 15.6** 3.2 ns 0.0 ns 2.7 ns 12.5** 6.4** 6.3** 4.0* 8.6** 9.1** 4.0* 0.7 ns 52.0** 55.3** 2.9 ns 0.5 ns 8.9** 1.8 ns 1.6 ns
ns ns ns ns ns ns ns ns
IL x S 5.0** 2.6 0.29 2.4 1.6 7.0** 0.6 1.0 2.1 17.9** 15.3** 3.1* 2.5 20.6** 3.4* 9.0** 6.6** 6.1** 2.7 ns
AxS 887.2** 366.2** 10.3** 497.1** 55.7** 11.4** 0.8 ns 116.4** 80.1** 10.4** 75.8** 55.1** 74.3** 261.8** 87.9** 16.3** 15.8** 4.5* 13.7**
IL x A x S 9.1** 4.5** 1.5 ns 3.0* 4.8** 2.0 ns 0.6 ns 6.3** 5.1** 14.5** 9.2** 8.7** 3.6* 45.7** 13.3** 7.6** 5.6** 1.7 ns 6.3**

ns non-significant effect, Level of significance: *P ≤ 0.05; **P ≤ 0.01; A photosynthesis rate, gs stomatal conductance, Ci internal C
­ O2 concentration, E transpiration rate, Pro proline, Carb
soluble carbohydrates, N-amino soluble amino acids
Page 7 of 18
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Page 8 of 18

Table 3  Pearson's correlation matrix for soil and plant analysis (C. prunifera), in the areas of Catuana and Minguaú
SM ECe ESP A gs Ci E Pro Carb N-amino N P K Mg Na Cl Na/K Fe

SM 1
ECe 0.76** 1
ESP 0.73** 0.99** 1
A 0.09 − 0.10 − 0.09 1
gs 0.28 0.07 0.08 0.92** 1
Ci 0.58** 0.56** 0.58** 0.09 0.41 1
E 0.33 0.16 0.17 0.88** 0.97** 0.46* 1
Pro 0.50* 0.73** 0.74** 0.16 0.29 0.60** 0.34 1
Carb 0.11 0.60** 0.63** − 0.30 − 0.20 0.24 − 0.19 0.59** 1
N-amino 0.15 0.21 0.21 − 0.72** − 0.49* 0.40 − 0.47* 0.04 0.40 1
N − 0.11 − 0.02 − 0.01 0.76** 0.55* − 0.18 0.57** 0.25 − 0.12 − 0.86** 1
P 0.04 0.19 0.21 0.57** 0.61** 0.29 0.60** 0.36 0.14 − 0.41 0.53* 1
K − 0.47* − 0.69** − 0.70** 0.25 0.01 − 0.61** − 0.01 − 0.34 − 0.48* − 0.39 0.26 − 0.06 1
Mg 0.58** 0.53* 0.54* 0.18 0.34 0.37 0.39 0.33 0.17 − 0.15 0.03 0.18 − 0.55** 1
Na 0.37 0.77** 0.79** − 0.29 − 0.07 0.58** 0.04 0.73** 0.73** 0.39 − 0.15 0.20 − 0.67** 0.40 1
Cl 0.49* 0.88** 0.89** − 0.27 − 0.12 0.47* − 0.06 0.69** 0.78** 0.33 − 0.12 0.23 − 0.63** 0.37 0.79** 1
Na/K 0.32 0.73** 0.75** − 0.30 − 0.06 0.58** 0.05 0.62** 0.65** 0.37 − 0.20 0.19 − 0.71** 0.46* 0.97** 0.76** 1
Fe 0.18 0.68** 0.71** − 0.44 − 0.25 0.44 − 0.18 0.60** 0.83** 0.46* − 0.27 0.08 − 0.68** 0.35 0.91** 0.81** 0.91** 1

Level of significance: *P ≤ 0.05; **P ≤ 0.01; SM soil moisture, ECe electrical conductivity of the saturation extract, ESP exchangeable sodium percentage, A photosynthesis rate, gs stomatal
conductance, Ci internal ­CO2 concentration, E transpiration rate, Pro proline; Carb soluble carbohydrates, N-amino soluble amino acids
Acta Physiologiae Plantarum
(2023) 45:41
 Acta Physiologiae Plantarum

Table 4  Pearson's correlation matrix for soil and plant analysis (C. madagascariensis), in the areas of Catuana and Minguaú
SM ECe ESP A gs Ci E Pro Carb N-amino N P K Ca Mg Na Na/K Cl Fe

SM 1
(2023) 45:41

ECe 0.76** 1
ESP 0.73** 0.99** 1
A 0.41 0.13 0.15 1
gs 0.26 − 0.09 − 0.07 0.96** 1
Ci 0.34 0.07 0.09 0.84** 0.87** 1
E 0.26 − 0.06 − 0.04 0.95** 0.98** 0.86** 1
Pro − 0.17 − 0.23 − 0.26 − 0.63** − 0.55** − 0.52* − 0.55** 1
Carb − 0.62** − 0.72** − 0.72** − 0.24 − 0.12 − 0.17 − 0.12 0.03 1
N-amino 0.26 − 0.02 − 0.02 0.44 0.40 0.33 0.46* − 0.04 − 0.08 1
N 0.59** 0.56** 0.58** 0.77** 0.61** 0.59** 0.63** − 0.51* − 0.41 0.42 1
P 0.67** 0.54** 0.56** 0.78** 0.63** 0.63** 0.66** − 0.57** − 0.44 0.55** 0.85** 1
K 0.25 − 0.26 -0.27 0.73** 0.79** 0.61** 0.76** − 0.32 0.00 0.60** 0.39 0.43 1
Ca − 0.70** − 0.64** − 0.65** − 0.75** − 0.61** − 0.62** − 0.63** 0.50* 0.60** − 0.32 − 0.87** − 0.81** − 0.41 1
Mg − 0.44 − 0.43 − 0.46* − 0.69** − 0.57** − 0.55** − 0.56** 0.59** 0.37 − 0.18 − 0.82** − 0.69** − 0.32 0.83** 1
Na 0.54* 0.92** 0.92** − 0.02 − 0.23 − 0.05 − 0.17 − 0.06 − 0.65** − 0.07 0.48* 0.34 − 0.41 − 0.53* − 0.36 1
Na/K 0.29 0.74** 0.76** − 0.20 − 0.36 − 0.12 − 0.29 0.06 − 0.47* − 0.26 0.30 0.14 − 0.65** − 0.28 − 0.23 0.89** 1
Cl 0.18 0.59** 0.61** − 0.11 − 0.25 − 0.24 − 0.21 0.05 − 0.47* -0.08 0.35 0.19 − 0.41 − 0.23 − 0.23 0.73** 0.77** 1
Fe 0.30 0.15 0.14 0.13 0.14 0.20 0.18 0.24 − 0.25 0.40 0.14 0.17 0.41 − 0.28 0.07 0.12 − 0.03 0.02 1

Level of significance: *P ≤ 0.05; **P ≤ 0.01; SM soil moisture, ECe electrical conductivity of the saturation extract, ESP exchangeable sodium percentage, A photosynthesis rate, gs stomatal con-
ductance, Ci internal ­CO2 concentration, E transpiration rate, Pro proline, Carb soluble carbohydrates, N-amino soluble amino acids
Page 9 of 18
41

13
 41 Page 10 of 18
Fig. 3  Principal Component Analysis (PCA) for soil and plant traits
in C. prunifera a and C. madagascariensis b depending on levels
of infestation (IL), experimental areas (Catuana and Minguaú) and
sampling periods (dry and rainy). KMO test: 0.698 and 0.701; Bar-
tlett's test: 153 and 171 (p < 0.05) respectively for C. prunifera and
C. madagascariensis. ECe electrical conductivity of the saturation
extract, ESP exchangeable sodium percentage, A photosynthesis rate,
gs stomatal conductance, Ci internal ­CO2 concentration, E transpira-
tion rate, Pro proline, Carb soluble carbohydrates, N-amino soluble
amino acids
levels x area x season) for almost all variables analyzed in
C. prunifera and C. madagascariensis. We then evaluated
this high complexity using the Pearson correlation matrix
and multivariate analyses.
Pearson’s correlation coefficients for C. prunifera
(Table 3) show that soil moisture, electrical conductivity
(ECe) and exchangeable sodium percentage (ESP) are posi-
tively correlated with each other. These soil parameters show
a negative correlation with the leaf K concentration and ECe
and ESP show a positive correlation with Na, Cl, Mg, Na/K
13
Acta Physiologiae Plantarum (2023) 45:41
ratio, Fe, internal C­ O2 concentration, and concentrations
of proline and carbohydrates. The sodium concentrations
show a strong positive correlation with the concentrations
of proline and carbohydrates and a negative correlation with
the K concentration. Photosynthesis rate and stomatal con-
ductance show a positive correlation with leaf N and P con-
centrations. Strong positive correlations were also observed
between stomatal conductance (gs), photosynthetic rate (A)
and transpiration (E).
Pearson’s correlation coefficients for C. madagascarien-
sis (Table 4) indicate that the soil variables have positive
correlation with the leaf N, P, Na, Cl and Na/K ratio, and
a negative correlation with leaf concentrations of calcium
and carbohydrates. Gas exchange was in positive correlation
with the leaf N, P and K concentrations and a negative cor-
relation with proline, Ca, and Mg concentrations.
The principal component analysis (Fig. 3) illustrates the
relationships between soil traits and the physiological, bio-
chemical, and nutritional responses measured in C. prunifera
(Fig. 3a) and C. madagascariensis (Fig. 3b), in relation to
infestation levels, experimental location and sampling sea-
son (rainy or dry). The PCA made it possible to obtain two
principal components with an eigenvalue greater than 1 for
C. prunifera and C. madagascariensis, which explain 67%
and 65% of the evaluated data, respectively (Fig. 3).
For C. prunifera (Fig. 3a), the first component (with an
eigenvalue of 7.7) has a strong association between ECe
(− 0.91), ESP (− 0.92), proline (− 0.66), carbohydrates
(− 0.71), K (0.75), Na (− 0.92), Cl (− 0.90), Na/K ratio
(− 0.89) and Fe (− 0.87). The photosynthetic rate (− 0.89),
stomatal conductance (− 0.91), transpiration (− 0.92), nitro-
gen (− 0.70), and soluble amino acids (0.64) are related to
the second component (eigenvalue of 4.4).
For C. madagascariensis (Fig. 3b), the first component
(eigenvalue of 7.1) showed a strong association between
soil moisture (0.71), photosynthetic rate (0.84), stomatal
conductance (0.71), intercellular C­ O2 concentration (0.55),
transpiration (0.73), N (0.88) and P (0.86). The second com-
ponent (eigenvalue of 5.3) presented a strong association
between ECe (− 0.76), ESP (− 0.76) and K (0.72).
Hierarchical clustering allowed the identification of six
clusters for C. prunifera (Fig. 4a) and four clusters for C.
madagascariensis (Fig. 4b). For C. madagascariensis, the
four clusters clearly distinguish the sampling locations and
season. Catuana, which has the greatest differences in soil
moisture between the dry and rainy seasons, forms clusters
1 and 4, which have great differences especially in terms of
leaf gas exchange. Minguaú, which differs in salinity and
has a small variation in soil moisture between the sampling
seasons, forms clusters 2 and 3, with significant differences
in biochemical and nutritional responses in the different
seasons. For C. prunifera, the four clusters also distinguish
the two locations and the two seasons. Unlike the invasive
Acta Physiologiae Plantarum (2023) 45:41 Page 11 of 18 41

Fig. 4  Dendrogram resulting

from cluster analysis with data
obtained in experimental areas,
sampling periods and infestation
levels (1–5) for C. prunifera
a and C. madagascariensis b.
A1 = Catuana Area; A2 = Min-
guaú Area; P1 = Rainy season;
P2 = Dry period

species, there are no greater dissimilarities between the
clusters of the same location, with clusters 2 and 5 repre-
senting Minguaú and clusters 4 and 6 representing Catuana.
However, there were two additional clusters for C. prunifera,
related to the treatments with the highest infestation level
(clusters 1 and 3, Fig. 4a), which were not verified for the
invasive species.
Leaf gas exchange and nitrogen concentration
Leaf gas exchange and nitrogen concentration were influ-
enced by the interaction between location, season and
infestation level (p < 0.01; Table 2). The two species
showed a similar trend (Fig. 5), with the highest values
of A and gs in Catuana during the rainy season. In the
dry season, this location had the largest reductions, with

13
 41 Page 12 of 18
Fig. 5  Photosynthesis-A (a, b) and stomatal conductance-gs (c, d)
in leaves of C. prunifera and C. madagascariensis as a function of
infestation level, experimental area (Catuana and Minguaú) and sam-
pling period (dry and rainy). Error bars represent standard error of the
mean (n = 3). Bars with the same letters for the same infestation level
a sharp decline in the values of A and gs, mainly in C.
madagascariensis (approx. 80% reduction in photosyn-
thetic rate). In Minguaú, these reductions were smaller
or nonexistent.
Inhibition of leaf gas exchange was observed in C.
prunifera, especially at the highest level of infestation,
with a 60.5% and 49.8% reduction in photosynthetic rate
in Catuana in the rainy and dry periods, respectively,
and a 66.71% and 82.44% reduction in Minguaú, when
compared to the control treatment (without infestation)
(Fig. 5a, c). However, at the low and intermediate lev-
els of infestation, there were significant reductions in leaf
gas exchange in Catuana (infestation levels 3 and 4) and
Minguaú (infestation levels 2, 3 and 4). For infestation
level 3, the photosynthetic rate (A) decreased during the
rainy season (12.7% in Catuana and 10.1% in Minguaú)
and especially during the dry season (A values decreased
by 21.5% in Catuana and 34.1% in Minguaú). Interaction
with C. prunifera showed no clear downward trend on leaf
13
Acta Physiologiae Plantarum (2023) 45:41
do not differ statistically by LSD test (p < 0.05). *Indicates a signifi-
cant difference by the LSD test (p < 0.05) in relation to the control
treatment (without infestation), for each location and season. Least
statistical difference (t test): a (1.16); b (1.57); c (0.05) and d (0.04)
gas exchange of C. madagascariensis, except in Minguaú
during the dry season (Fig. 5b, d).
The nitrogen concentrations in the leaves show marked
differences between the native and invasive species
(Fig. 6). For the native species, the leaf nitrogen concen-
tration only decreases at the highest level of infestation,
regardless of the location and sampling season (Fig. 6a).
The invasive species shows a lower N concentration in the
dry season in Catuana, regardless of the infestation level
(Fig. 6b), which is indicative of the senescence process
occurring in the leaves that remain after a reduction in
soil moisture (Fig. 1). The N concentration in C. mada-
gascariensis is not impacted by infestation level nor by the
sampling season in the Minguaú location, which has a high
soil moisture content, even in the dry season.
Acta Physiologiae Plantarum (2023) 45:41
Fig. 6  Nitrogen concentrations in leaves of C. prunifera a and C.
madagascariensis b as a function of infestation level, experimental
area (Catuana and Minguaú) and sampling period (dry and rainy).
Error bars represent standard error of the mean (n = 3). Bars with the
same letters for the same infestation level do not differ statistically by
LSD test (p < 0.05). *Indicates a significant difference by the LSD
test (p < 0.05) in relation to the control treatment (without infesta-
tion), for each location and season. Least statistical difference (t test):
a (1.35); b (1.89)
Sodium and chloride concentrations
Leaf concentrations of sodium and chloride were affected
by the interaction between location, season, and infesta-
tion level (p < 0.01; Table 2). In general, sodium concen-
trations were much higher in C. madagascariensis than
in C. prunifera (Fig. 7), indicating that the two species
have different mechanisms of coping with the salinity and
sodicity constraints. Regardless of the species, higher
levels of sodium and chloride were found in the plants
growing in Minguaú, especially during the dry season,
which is explained by the high ECe and ESP of the soil
(Table 1), in comparison to Catuana. When comparing
infestation levels, an 86% increase in sodium concentra-
tion was observed in C. prunifera at the highest infestation
Page 13 of 18 41
level during the dry season (Fig. 7a), a value much higher
than observed for C. madagascariensis, which reached
only 49% (Fig. 7b).
Discussion
Thousands of carnauba palm trees grow in extensive
areas of Alfisols and alluvial soils in northeastern Bra-
zil (Arruda and Calbo 2004; Andrade 2013), and these
carnauba populations have been exploited by extraction
to obtain various products, especially the wax that cov-
ers their leaves (Pereira et al. 2014; Moro et al. 2015).
The establishment of C. prunifera in these soils indicates
that it has mechanisms by which to adapt to water excess
or shortage. However, our results demonstrate that the
invasive species C. madagascariensis has high pheno-
typic plasticity and different mechanisms of adaptation,
enabling it to compete with C. prunifera under different
soil abiotic restrictions. C. madagascariensis has a greater
competitive advantage in flooded areas, as shown by the
highest relative infestation index (52%). In non-flooded
areas, the invasive species loses its leaves during the dry
season (Supplementary material S2), also confirming its
ability to survive in a semi-arid tropical climate. The loss
of leaves in the invasive species delays growth and reduces
the relative infestation in non-flooded areas, as observed
in the present study.
Our results show that the dynamics of facilitation and
competition are present in the interaction between C. prunif-
era and C. madagascariensis, with a clear predominance
of competition mechanisms. There was no evidence of
facilitation in terms of shading in the initial stage or soil
modifications promoted by C. prunifera that could benefit
the invasive plant. However, the upright stem of the palm
facilitates and enhances the growth of C. madagascariensis
due to its climbing nature (Gianoli 2015; Sousa et al. 2016).
Under flooding and waterlogging conditions, such as those
observed in Minguaú, C. madagascariensis maintains a high
rate of photosynthesis, which favors rapid growth, making
it a strong competitor, as demonstrated by its formation of
dense vegetation in the floodable Alfisols of the Caatinga,
both in the presence and absence of C. prunifera.
The highest values of soil moisture are associated with
higher soil salinity and sodicity, which in turn result in a
greater accumulation of Na, Cl, proline, carbohydrates
and iron, and a reduction in potassium concentrations in
the leaves of C. prunifera, according to PCA. While the
accumulation of iron in plant leaves is a typical response
to flooded conditions (Schmidt et al. 2013; Krohling et al.
2016), the accumulation of potentially toxic ions (Na and Cl)
and organic solutes, and a reduction in potassium concen-
tration are clear responses to salt stress (Munns and Tester
13
 41 Page 14 of 18
Fig. 7  Sodium and chloride concentrations in leaves of C. prunifera
(a, c) and C. madagascariensis (b, d) as a function of infestation
level, experimental area (Catuana and Minguaú) and sampling period
(dry and rainy). Error bars represent standard error of the mean
(n = 3). Bars with the same letters for the same infestation level do not
2008; Wang et al. 2015; Marinoni et al. 2020). There is also
a strong association between photosynthesis rate and leaf N
concentration in C. prunifera, indicating that the decrease in
photosynthetic rate is due, at least in part, to the reduction
in N concentration, which results in a lower leaf chlorophyll
concentration.
The hierarchical clusters allowed a clear distinction of
the ecophysiological responses between the invasive spe-
cies and the native palm tree. C. prunifera shows the bet-
ter balance in the leaf responses as subjected to changes in
soil moisture throughout the year, especially in Catuana, as
showed by lower dissimilarities between clusters. However,
C. prunifera formed two other clusters which include the
highest levels of infestation, indicating that this treatment
results in high damage and lethality to the trees. Cluster 3
separates the highest level of infestation in Catuana (dry
and rainy seasons) and Minguaú (rainy season) and differed
13
Acta Physiologiae Plantarum (2023) 45:41
differ statistically by LSD test (p < 0.05). *Indicates a significant dif-
ference by the LSD test (p < 0.05) in relation to the control treatment
(without infestation), for each location and season. Least statistical
difference (t test): a (0.83); b (3.19); c (3.51) and d (3.62)
mainly due to the low photosynthetic rate and nitrogen con-
centrations. Cluster 1, on the other hand, was formed by the
treatment of the highest infestation (level 5) in the Minguaú
area, during the dry season, and its differentials were the low
concentrations of N, lower rates of photosynthesis, higher
values of Ci and greater accumulation of sodium, proline
and carbohydrates, responses commonly observed under salt
stress conditions (Santos et al. 2020). On the other hand, the
invasive species does not form clusters related to infestation
levels, indicating that the impacts of the interaction on eco-
physiological responses were much smaller when compared
to the effects on the native species.
The photosynthesis rates of C. prunifera under permanent
shading were lower in the high soil salinity (Minguaú), that
is, in the most stressful environment. Otherwise, low values
of A and high values of Ci observed during the dry season
in the same area suggest the occurrence of a non-stomatal
effect on the photosynthetic process (Ren et al. 2016; Lac-
erda et al. 2020), indicating that permanent shading caused
Acta Physiologiae Plantarum (2023) 45:41
by the invasive species impacts the photochemical and bio-
chemical apparatus, and these effects are intensified by soil
abiotic constraints. It is probable that the competitive capac-
ity of C. prunifera decreases as salt stress intensifies, since
the increased energy investment required to tolerate excess
salt leads to a reduced investment in competitive ability,
known as a tolerance-competition trade-off (Schoolmaster
and Stagg 2018).
Cluster analysis doesn’t identity an effect of the invasive
species on nutrient concentration (except for N) that would
affect the growth and development of C. prunifera. However,
the reduction in N concentration may be a consequence of
leaf senescence induced by shading, which results in the
translocation of nitrogen compounds, rather than reduced
absorption of nitrogen from the soil. This suggests that the
interaction between C. prunifera and C. madagascariensis
is defined by the level of soil abiotic restrictions (salinity,
sodicity, water-deficit and excess) rather than by competition
for essential mineral resources present in the soil. However,
the reduction in stomatal conductance and photosynthetic
rate observed in C. prunifera leaves at an intermediate level
of infestation may indicate competition with C. madagas-
cariensis for soil water, which can also reduce the amount
of nutrients absorbed by mass flow.
Interaction with C. prunifera caused reductions in leaf
gas exchange in C. madagascariensis in Minguaú during the
dry season, when an increase in soil salinity was observed.
However, C. madagascariensis had high photosynthetic
rates even in leaves with a high sodium concentration, evi-
dence that this invasive species is tolerant to the direct and
indirect effects of salts, as defined by Rengasamy (2016).
This result also demonstrates the high competitiveness of
this species in sodic soils, which are common in the Brazil-
ian semi-arid region (Albuquerque et al. 2018) and have low
permeability and are flooded or waterlogged throughout the
year. According to Richardson and Pys̆ek (2006), a wide
range of environments are invaded by exotic species because
most of them have high phenotypic plasticity. The ability
to modify morphological, physiological, anatomical, and
growth characteristics to withstand environmental changes
(Miner et al. 2005), explains the occurrence of C. madagas-
cariensis in moist or dry soils with different levels of salinity
and sodicity (Brito et al. 2015).
The photosynthetic responses of the two species also
show interesting aspects in terms of tolerance to soil
constraints, especially moisture and salinity. Carnauba
trees have a higher photosynthetic rate than the invasive
species in the dry season in Catuana, when there is a
strong reduction in soil moisture. The palm trees keep
their leaves intact, accumulate wax on the leaf surfaces
and control stomatal opening, reducing transpiration rates
and net C­ O2 assimilation. In contrast, C. madagascarien-
sis loses its leaves, and the photosynthesis rate decreases
Page 15 of 18 41
by about 80% in the remaining leaves, indicating that is
has greater sensitivity to severe water-deficit.
Stress factors associated with low soil moisture and salinity
increase the metabolic costs of maintenance and reduce leaf
gas exchange in perennial species (Munns and Tester 2008;
Medri et al. 2012; Medeiros et al. 2018; Santos et al. 2020).
In the rainy season, the photosynthesis rates are, in general,
higher in both species in the Catuana area, which can be
explained by the absence of stress factors. In both species,
the reduction in the rate of photosynthesis in the dry season is
much lower in high soil moisture conditions (Minguau), than
in conditions of a prolonged water-deficit (Catuana), indicating
that both species can tolerate different soil constraints (Brito
et al. 2015; Singh 2015). Arruda and Calbo (2004) found that
soil flooding had little impact on photosynthesis and stomatal
conductance and did not affect shoot growth or induce the
appearance of visual symptoms in C. prunifera, indicating that
it is tolerant to flooding, possibly due to the high porosity of
its roots.
Conclusions
Our results show that the competitive interaction between
C. prunifera and C. madagascariensis is mainly defined by
their adaptability to soil abiotic constraints. The native spe-
cies C. prunifera is better adapted to severe water-deficit
conditions, but its ecophysiological performance is not suf-
ficient to maintain the carnauba populations in the Caatinga
ecosystem since the introduction of C. madagascariensis.
This invasive species loses its leaves during the dry sea-
son, especially in non-flooded areas, showing high capac-
ity for survival in hot semi-arid environments. However, in
waterlogged conditions in salt-affected soils, C. madagas-
cariensis becomes more competitive and its ecophysiologi-
cal responses are not severely impacted, even with a high
accumulation of sodium in its leaves, showing that increased
salt stress does not hinder the invader. Our results also show
that the negative impacts on C. prunifera occur specifically
in the final stage of infestation, when shading caused by the
invader restricts access to solar radiation and accelerates leaf
senescence, confirmed by the reduction in nitrogen concen-
tration and photosynthetic rate. However, the impacts on the
native species precede the permanent shading, as evidenced
by the inhibition of net assimilation of ­CO2 under intermedi-
ate levels of infestation, associated with competition for soil
water. Together, these results demonstrate that an increase in
water resources benefit the invasion and reinforce the vulner-
ability of carnauba populations of the Caatinga ecosystem,
which may be severely impacted without the development of
technologies to control the invasive species and to mitigate
the impacts on the invaded ecosystem. Further studies on the
development of the root system in flooded and non-flooded
13
 41 Page 16 of 18
areas are also necessary for a better understanding of the
competitive interaction between these two species.
Author contributions statement WJFM, CFL, CHCS, AAR,
and RSB performed all soil and plant sampling in the field.
CFL and CHCS performed leaf gas exchange measurements.
WJFM, AAR and RSB performed all laboratory analyses
(plant and soil). WJFM, ICSA and AMEB performed statis-
tical data analyses for all soil and plant traits. The first draft
of the manuscript was written by WJFM, CFL, RBZ, ICSA
and AMEB. CFL and RBZ reviewed this draft in several
rounds. All authors agree on the content of this manuscript.
Supplementary Information The online version contains supplemen-
tary material available at https://d​ oi.o​ rg/1​ 0.1​ 007/s​ 11738-0​ 23-0​ 3525-8.
Acknowledgements Acknowledgments are due to the Brazilian
National Council for Scientific and Technological Development
(CNPq), ‘National Institute of Science and Technology in Salinity
(INCTSal)’, The Coordination for the Improvement of Higher Level
Personnel Agency (CAPES), the ‘Ceará State Development Agency
(ADECE)’, Brazil, The Cearense Foundation to Support Scientific and
Technological Development (FUNCAP), and Secretariat for Economic
Development and Labor (SEDET), for financial support provided for
this research and award of fellowship to the first author (CAPES). Part
of the data comes from particular PhD Thesis by Wiliana Julia Ferreira
de Medeiros (first author), entitled “Impactos de fatores do solo e da
competição com Cryptostegia madagascariensis sobre as respostas
ecofisiológicas de plantas jovens e adultas de Copernicia prunifera”,
and deposited in https://​repos​itorio.​ufc.​br/​handle/​riufc/​62553.
Data availability Not applicable for that section.
Code availability Not applicable for that section.
Declarations
Conflicts of interest The authors declare that they have no competing
interests.
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