Article

Analysis of Associated Woody and Semi-Woody Local Wild

Species in Entre Ríos, Argentina: Exploring the Agricultural
Potential of Hexachlamys edulis
Ignacio Sebastián Povilonis 1,2, * , Miriam Elisabet Arena 1,2 , Marta Alonso 2 and Silvia Radice 1,2

1 National Scientific and Technical Research Council (CONICET), Godoy Cruz 2290, C1425 FQB, Argentina;
miriamearena@gmail.com (M.E.A.); siradice@yahoo.com (S.R.)
2 Laboratorio de Fisiología Vegetal, Universidad de Morón, Machado 914, Lab 501,
Morón B1708EOH, Argentina; giudicimarta@gmail.com
* Correspondence: ipovilonis@unimoron.edu.ar

Abstract: The loss of native forests in Argentina has been a concern, driven by factors such as agri-
culture expansion and urbanization. Therefore, understanding the conservation status of sampled
populations and their adaptation to different plant communities is essential. This research focused on
the heterogeneity analysis of the associated woody and semi-woody vegetation to Hexachlamys edulis
(O. Berg) Kausel and D. Legrand, a species commonly known as “ubajay” in Entre Ríos, Argentina.
The study aimed to record the species present in the populations, explore plant communities associ-
ated with H. edulis, identify other potentially useful agroforestry species, compare locations based
on the similarity of accompanying species, and explain the conservation status of each population.
Results revealed a total of 71 species belonging to 39 families. The Myrtaceae family was the most
relevant, particularly in terms of native species representation. The analysis of biodiversity indicators,
including richness, the Shannon index, and dominance revealed variations among the studied sites.
The anthropic indicator highlighted the impact of human activity, with Concordia showing a higher
ratio of native-to-exotic species. Cluster analysis and ordination techniques revealed groupings of
censuses from the same localities, indicating differences in vegetation composition between sites.
Citation: Povilonis, I.S.; Arena, M.E.;
Significant differences in species composition were found among the sampled populations. Overall,
Alonso, M.; Radice, S. Analysis of
the study can serve as baseline information for future research on the dynamics of vegetation in
Associated Woody and Semi-Woody
these areas and on the studied H. edulis species. Finally, these findings contribute to understanding
Local Wild Species in Entre Ríos,
how wild species like H. edulis adapt to different plant communities, which might be valuable for
Argentina: Exploring the Agricultural
Potential of Hexachlamys edulis.
developing new agroecological approaches or identifying potential companion planting species in
Sustainability 2024, 16, 10029. https:// future agricultural systems.
doi.org/10.3390/su162210029
Keywords: native forest; biodiversity; multivariate analysis; agroforestry; Myrtaceae
Academic Editor: María
Pilar González-Hernández

Received: 2 September 2024

Revised: 13 November 2024 1. Introduction
Accepted: 14 November 2024 Native forests and biodiversity play a pivotal role in ecological, economic, and social
Published: 17 November 2024
sustainability. From an environmental perspective, they act as carbon sinks, helping to
reduce the amount of carbon dioxide in the atmosphere. They protect the soil from erosion
and maintain the water quality of wetlands and rivers. Also, native forests provide valuable
Copyright: © 2024 by the authors.
ecosystem services [1]. These services include hosting insect pollinators, purifying the air,
Licensee MDPI, Basel, Switzerland. mitigating the effects of floods, storms, and noise pollution [2], and stabilizing dunes in
This article is an open access article desert areas [3], among others. Indeed, links have been demonstrated between biodiversity
distributed under the terms and and improvements in objective measures of health and well-being [4]. Even today, many
conditions of the Creative Commons Indigenous Peoples and Local Communities rely on native forests as a source of food and
Attribution (CC BY) license (https:// medicine in addition to their cultural value [5].
creativecommons.org/licenses/by/ The ecological stability of native forests depends on biodiversity; therefore, they are
4.0/). essential for maintaining a healthy and balanced ecosystem, and their conservation is

Sustainability 2024, 16, 10029. https://doi.org/10.3390/su162210029 https://www.mdpi.com/journal/sustainability

Sustainability 2024, 16, 10029 2 of 17

crucial to ensure the availability of resources and services for future generations. In this
regard, it is necessary to take measures to protect and conserve them. This can be achieved
through the creation of protected areas, the implementation of sustainable agricultural
and livestock practices, and the promotion of environmental education and awareness
among the population. Without immediate action, these areas and their biodiversity are at
risk of degradation or even permanent loss, as they harbor endemic organisms that are at
risk of extinction. Success or failure will depend on international cooperation efforts such
as the Kunming-Montreal Global Biodiversity Framework [6] and the Forests, Trees, and
Agroforestry Partnership [7], as well as the actions of each and every one of us.
Local wild species are essential for informing sustainable management practices and
developing innovative, resilient, and sustainable agricultural systems, thus contributing to
the well-being of communities and the conservation of our natural heritage. Integrating
knowledge of biodiversity into forest management strategies allows for the design of
practices that conserve and enhance these ecosystems. For example, identifying and
protecting key plants and animals can foster the natural regeneration of the forest and
long-term sustainability. Additionally, research on ecological interactions and biological
processes and the detection of key indicators provides crucial information for the restoration
of degraded areas, the creation of biological corridors that connect fragmented habitats,
and the incorporation of new species into cropping systems [8].
Despite their importance, the area of native forests in Argentina has suffered a loss of
6,631,000 hectares between the years 1990 and 2020. In 2020, an estimated 27,137,000 hectares of
native forests were recorded, which represents 10.28% of the country’s total land area [9].
The main causes of deforestation are attributed to the expansion of agriculture, livestock
farming, and urbanization [10,11]. In particular, this fact coincides with the global trend
of a dramatic acceleration in cropland expansion within protected areas from 2000 to
2019 [12]. In general, these advances in conserved areas and human activity result in
biodiversity loss and the introduction of exotic species. Identifying the introduced taxa
and understanding how native species adapt to human environments provides valuable
insights into ecosystem functioning, invasion patterns, and resilience. This highlights the
importance of assessing the environmental quality of all species, especially non-native ones,
to fully understand how ecosystems are impacted by human activity. However, despite
this situation, there are still areas with low anthropogenic impact, as is the case with the
riparian forest along the Uruguay River in the province of Entre Ríos. These areas are
crucial for biodiversity due to the vegetation intrusion phenomenon, in which species from
the Paranaense Province migrate southward through the Uruguay and Paraná Rivers and
adapt to the riparian microclimate [13,14]. In fact, this situation results in an increase in
heterogeneity and diversity within and between species and ecosystems, respectively. Mass
effect, the occurrence of species outside their core habitats, could also be explained by this
phenomenon [15].
A species that stands out in these areas is Hexachlamys edulis (O. Berg) Kausel and D.
Legrand, commonly known as “ubajay.” This species is found in areas near watercourses
and riparian forests along the Paraná and Uruguay Rivers. Furthermore, it is notable
for its edible fruit and its potential as a non-timber forest resource of importance for
health and nutrition. Without a doubt, H. edulis stands out as a promising species for
incorporation into cropping systems to enhance biodiversity and promote sustainable
agricultural practices [16–20].
Within the framework of studies on the phenotypic variability of H. edulis, which
is necessary for subsequent breeding and domestication efforts, it is essential to under-
stand the conservation status of the sampled populations. This understanding can help
assess the potential risks faced by this species and determine whether H. edulis popula-
tions coexist with different woody and semi-woody plant communities. According to
Llorente–Culebras et al. [21], woody plants were the most frequently studied group in
global biodiversity research on protected areas, and these communities support numerous
other species while significantly contributing to local biodiversity [22].
Sustainability 2024, 16, 10029 3 of 17

H. edulis exhibits remarkable adaptability to the riparian ecosystems of the Paraná and
Uruguay Rivers, where its nutritional value of the edible fruit position it as a promising
candidate for agroforestry systems. By integrating H. edulis into cropping systems, we
can enhance biodiversity, promote soil health, and provide a sustainable source of non-
timber forest products. Its presence within diverse plant communities opens avenues to
investigate ecological interactions with both native and exotic species, thereby enriching our
understanding of local biodiversity dynamics. This study aims to evaluate the conservation
status and agroforestry potential of H. edulis within these ecosystems, filling a significant
research gap, as few studies in the region have addressed this, with the exception of the
study in NP El Palmar [23].
The objectives of this study are fivefold: (1) to document the species and families
present in the habitats where H. edulis grows, focusing on other species with potential
agroforestry applications; (2) to analyze biodiversity indicators within the woody and
semi-woody communities associated with H. edulis; (3) to assess the conservation status
of each population based on the ratio of native-to-exotic species; (4) to compare different
locations by examining the similarity of woody and semi-woody species accompanying
H. edulis trees, specifically exploring species richness to determine the occurrence of H.
edulis across various plant communities; and (5) to recommend other outstanding species
in the populations under study for introduction into agroforestry systems.

2. Materials and Methods

2.1. Plant Material and Studied Populations
In September 2019, a total of 40 adult trees of H. edulis with a diameter at breast
height greater than 7.5 cm were randomly selected from three populations in the riparian
forest along the Uruguay River in Entre Ríos (Figure 1), ensuring that they were spaced
more than 5 m apart and not dead. The labeled individuals ranged from 154 to 208 in
Concordia, from 260 to 288 in National Park (NP) El Palmar, and from 305 to 364 in
Gualeguaychú, covering an approximate area of 300 km2 . Specifically, 12 individuals
were selected in Concordia (76 hectares, −31.28590 S: −57.96305 W; IUCN category not
reported), 15 in NP El Palmar (150 hectares, −31.86395 S: −58.20998 W; IUCN category
II), and 13 in the private reserve El Potrero de San Lorenzo in Gualeguaychú (16 hectares,
−33.06490 S: −58.26965 W; IUCN category VI) [24]. A radius of 3 m around each selected
H. edulis tree was established to record and count accompanying woody and semi-woody
perennial species, ensuring a minimum surveyed area of 28.3 m2 , followed
Sustainability 2024, 16, x FOR PEER REVIEW 4 of 19
by the taxonomic
classification and documentation of all species present.

Figure 1. Figure 1. Geographic location of the three study sites along the Uruguay River in the province of
Geographic location of the three study sites along the Uruguay River in the province
Entre Ríos, Argentina. The sites include Concordia, National Park (NP) El Palmar, and the private
of Entre Ríos, Argentina.
reserve El Potrero de The sites include
San Lorenzo Concordia,
in Gualeguaychú. The leftNational
map shows Park (NP)
the general El Palmar,
location in and the private
South America, while the right map details the specific position of each site in relation to the Uru-
guay River.
 Sustainability 2024, 16, x FOR PEER REVIEW 4 of 19

Sustainability 2024, 16, 10029 4 of 17

reserve El Potrero de San Lorenzo in Gualeguaychú. The left map shows the general location in South
America, while the right map details the specific position of each site in relation to the Uruguay River.

These sites had experienced varying degrees of human disturbance, including agri-
culture and urban development. Furthermore, the study site in Concordia is surrounded
by recreational activities, including camping, local fishing visitors, and small productive
establishments, which may contribute to varying degrees of human disturbance. However,
NP El Palmar is comparatively more conserved, although it experiences some level of
anthropization due to tourism and camping activities. Lastly, in Gualeguaychú, the area is
relatively well-preserved, as it is not publicly accessible; however, there are nearby forestry
and beekeeping productions that may influence the local ecosystem dynamics.

2.2. Climate Characterization

The recorded
Figure 1. monthly average
Geographic location temperatures
of the three study sites and
along precipitation
the Uruguay Riverfor each
in the study
province of site
Entre Ríos, Argentina. The sites include Concordia, National Park (NP) El
between 1991 and 2021 are shown in Figures 2 and 3 [25]. Temperature and precipitation Palmar, and the private
reserve El Potrero de San Lorenzo in Gualeguaychú. The left map shows the general location in
patterns provide valuable insights into the climatic conditions that influence the growth
South America, while the right map details the specific position of each site in relation to the Uru-
and distribution of H. edulis and other plant species in the area.
guay River.

Figure
Sustainability 2024, Figure 2.
Historical
2.PEER
16, x FOR REVIEW Historicalaverage
monthly monthly average
temperatures (◦ C)(°C)
temperatures between1991
between 1991 and
and2021
2021in in
Concordia,
5NP
of El
Concordia, 19NP El
Palmar, and Gualeguaychú. Dashed lines indicate historical annual average temperatures.
Palmar, and Gualeguaychú. Dashed lines indicate historical annual average temperatures.

Figure 3. monthly
Figure 3. Historical Historical monthly
averageaverage precipitationbetween
precipitation between 1991
1991and 20212021
and in Concordia, NP El Pal-NP El
in Concordia,
mar, and Gualeguaychú. Dotted lines indicate historical annual average precipitation.
Palmar, and Gualeguaychú. Dotted lines indicate historical annual average precipitation.
2.3. Biodiversity Indicators and Statistical Analysis
In addition to species richness as a primary measure of biodiversity [26] and to ad-
dress the complexity present in the structure of a plant community, various indicators
were employed, such as dominance, equitability, and evenness (Table 1).

Table 1. Formulas and breakdown of biodiversity and anthropic indicators used in the study. The
Sustainability 2024, 16, 10029 5 of 17

2.3. Biodiversity Indicators and Statistical Analysis

In addition to species richness as a primary measure of biodiversity [26] and to
address the complexity present in the structure of a plant community, various indicators
were employed, such as dominance, equitability, and evenness (Table 1).

Table 1. Formulas and breakdown of biodiversity and anthropic indicators used in the study. The table
outlines various indicators, including Shannon entropy, dominance, equitability, evenness, Margalef’s
index, and an anthropic indicator, along with their respective formulas and detailed breakdowns.

Indicator Formula Formula Breakdown

Calculate the sum of the product of each species’
Shannon H = −Σ(pi*log(pi))
abundance proportion (pi) and its logarithm.
Sum the squared proportions of each
Dominance D = Σ(piˆ2)
species’ abundance.
Divide the Shannon entropy (H) by the logarithm of the
Equitability J = H/log(S)
number of species (S).
Calculate the exponential of Shannon entropy (H)
Evenness eˆH/S = exp(H)/S
divided by the number of species (S).
Subtract 1 from the number of species (S) and divide it
Margalef M = (S − 1)/log(N)
by the logarithm of the total individuals (N).
Anthropic Divide the number of native species by the sum of
Ia = (n◦ natives)/(n◦ natives + n◦ exotics)
Indicator native and exotic species counts.

First, vegetal community structure was characterized by calculating species abundance

and species richness. The Shannon–Wiener index [27] of species diversity (H’), dominance
(D), Pielou equitability (J), evenness (eH /S), and Margalef index (M) were also calculated at
each site according to formulas in Table 1 using PAST 3.24 [28]. A distinction was made
between native and exotic species, and an anthropic indicator (Ia) was generated (adapted
from Nápoles) [29] to indicate the ratio of native-to-exotic species, where 1 indicates com-
pletely native vegetation and 0 indicates completely exotic vegetation. Prior to statistical
analyses, normality, and homogeneity of variances were assessed for the calculated de-
pendent variables using the Shapiro–Wilks and Levene tests. For each index, an analysis
of variance was conducted comparing the three study sites. General linear models were
used, either with variance adjustment by site or generalized linear models using a gamma
distribution with an identity link function as appropriate. Multiple comparison analyses
were performed using the Tukey test (p-value = 0.05).
Furthermore, to measure differences in species structure among the studied locations
and to compare the heterogeneity of the accompanying vegetation, a presence absence
matrix was created. First, species with occurrences of lower than 7.5% were removed. The
data were standardized through normalization, and then, the dissimilarity matrix was
calculated based on the Bray–Curtis index. Complementary clustering methods, such as
Ward’s merging algorithm for cluster analysis, which delivers mutually exclusive groups
where each group includes members with the highest similarity, providing maximum
internal homogeneity [30].
To conduct the Principal Coordinates Analysis (PCoA), we constructed a similarity
matrix based on the abundance of species across different censuses using the Bray-Curtis
index, which is particularly suitable for presence–absence and abundance data, as noted by
Palacio et al. [31]. This method allows for the ordering of sampling units according to a
measure of similarity that reflects the relationships within the data without imposing the
limitations of Principal Component Analysis. In the analysis, three dimensions (k = 3) were
determined to adequately represent the variability present in the data. The significance of
the principal coordinates was expressed as a percentage of the total variance explained,
enabling the interpretation of results based on the distribution of samples. The PCoA
Sustainability 2024, 16, 10029 6 of 17

results were visualized using scatter plots, where each point represents a sampling unit,
differentiated by population. Additionally, ellipses were included to visualize variability,
and labels were used to identify the censuses, facilitating the interpretation of the observed
patterns in species distribution across different sites.
Discriminant analysis was also performed, with Mahalanobis distances, to classify
groups based on selected ecological variables and to maximize the differences between
these groups. This analysis employed a canonical discriminant approach, allowing for
the identification of the linear combinations of predictor variables that best separate the
predefined groups. The significance was evaluated using multi-response permutation
procedures (MRPPs) with 1000 permutations and the Bray–Curtis distance method. All
data were analyzed using Rstudio [32].

3. Results
3.1. Biodiversity Indicators
The total flora of the studied areas was cataloged, revealing 39 families with a richness
of 71 species and an abundance of 613 individuals (Table A1 in Appendix A). Only four
species, all of them native, displayed absolute consistency and were found in the three sites:
Acacia caven, Allophylus edulis, Celtis tala, and Eugenia uruguayensis. The number of native
species with the highest fidelity, meaning that they only grow at each site, is six in Concordia
(Clematis montevidensis, Heterothalamus alienus, Mimosa pilulifera, Myrtus mucronatum, Pavonia
malvacea, and Stigmaphyllon bonarense), three in NP El Palmar (Myrrhinium atropurpureum,
Schinus molle, and Solanum jazminoides), and five in Gualeguaychú (Asparagus setaceus,
Buddleja globosa, Celtis iguanaea, Maytenus ilicifolius, and Myrsine laetevirens).
The individuals of the Myrtaceae family had the highest relevance, as it was the family
Sustainability 2024, 16, x FOR
with the PEER REVIEW
greatest representation of native species in Concordia and Gualeguaychú and the7 of 19

second highest in NP El Palmar, following the Anacardiaceae family (Figure 4).

Figure 4. Top Figure 4. Topand

five native fiveexotic
nativerichness
and exotic
of richness of each
each family in family in Concordia,
Concordia, NP El Palmar,
NP El Palmar, and and
Gualeguaychú. The family data are sorted according to each family’s importance in the overall studyoverall
Gualeguaychú. The family data are sorted according to each family’s importance in the
study and then by its importance in the locality.
and then by its importance in the locality.
The most frequent native species at the sites were Eugenia uruguayensis (17), Scutia
The most frequent native species at the sites were Eugenia uruguayensis (17), Scutia
buxifolia (15), and Allophylus edulis (13), while the most frequent exotic species were
buxifolia (15), and Allophylus edulis (13), while the most frequent exotic species were Ephedra
Ephedra twediana (9), Asparagus setaceus (8), and Juncus acutus (6) (Figure 5).
twediana (9), Asparagus setaceus (8), and Juncus acutus (6) (Figure 5).
The average number of individuals and species was significantly different between
Gualeguaychú (17.38 and 6.23) and NP El Palmar (10.00 and 4.29), while Concordia did
not show any differentiation (15.33 and 5.42, respectively). According to the Margalef
index, there are not statistical differences between populations (Figure 6). Equitability
was similar for the three populations, and the uniformity explained by evenness (eH /S)
for each site was also very similar. Dominance was significantly higher in NP El Palmar
(0.36) than in Gualeguaychú (0.22), although without differences with Concordia (0.28).
Sustainability 2024, 16, 10029 Figure 4. Top five native and exotic richness of each family in Concordia, NP El 7Palmar,
of 17 and
Gualeguaychú. The family data are sorted according to each family’s importance in the overall
study and then by its importance in the locality.

Also, the ecologicalThe

diversity calculated
most frequent using
native the Shannon–Weaver
species index shows
at the sites were Eugenia significant
uruguayensis (17), Scutia
differences between
buxifoliaNP El and
(15), Palmar (1.23) and
Allophylus edulisGualeguaychú
(13), while the (1.66). Lastly, the
most frequent anthropic
exotic species were
indicator valueEphedra
was 0.85 for Concordia,
twediana 0.78
(9), Asparagus for NP
setaceus (8),Eland
Palmar,
Juncusand 0.70
acutus (6)for Gualeguaychú.
(Figure 5).

Figure 5. Top five native5.and

Figure Topexotic
five species frequency
native and exotic inspecies
Concordia, NP ElinPalmar,
frequency and Gualeguaychú.
Concordia, NP El Palmar, and
Sustainability 2024, 16,The
x FOR dataGualeguaychú.
PEER REVIEW
species The species
are sorted according data
to the are sorted according
importance to the
of the family in importance
the overallof the family
study in the
and then ofoverall
8 by 19
study and then by its importance in the locality.
its importance in the locality.
The average number of individuals and species was significantly different between
Gualeguaychú (17.38 and 6.23) and NP El Palmar (10.00 and 4.29), while Concordia did
not show any differentiation (15.33 and 5.42, respectively). According to the Margalef in-
dex, there are not statistical differences between populations (Figure 6). Equitability was
similar for the three populations, and the uniformity explained by evenness (eH/S) for each
site was also very similar. Dominance was significantly higher in NP El Palmar (0.36) than
in Gualeguaychú (0.22), although without differences with Concordia (0.28). Also, the eco-
logical diversity calculated using the Shannon–Weaver index shows significant differ-
ences between NP El Palmar (1.23) and Gualeguaychú (1.66). Lastly, the anthropic indica-
tor value was 0.85 for Concordia, 0.78 for NP El Palmar, and 0.70 for Gualeguaychú.

Figure 6. Biodiversity index for

Figure 6. Biodiversity each
index forsite. Different
each site. letters
Different above
letters aboveeach barindicate
each bar indicate significant
significant differ-
differences for each index according to Tukey’s test (p ≤ 0.05). Bars display the standard deviationof
ences for each index according to Tukey’s test (p ≤ 0.05). Bars display the standard deviation ofthe
mean values.
the mean values.
3.2. Multivariate Analisys
Cluster analysis (Figure 7) shows a grouping of the censuses into three clusters. Each
cluster is represented by the censuses from each population, except for 288, 305, 306, 321,
281, and 285. This means that 85% of the censuses are grouped within the censuses from
the same population. NP El Palmar and Gualeguaychú show a lower distance explained
by vegetation composition.
Sustainability 2024, 16, 10029 8 of 17

3.2. Multivariate Analisys

Cluster analysis (Figure 7) shows a grouping of the censuses into three clusters. Each
cluster is represented by the censuses from each population, except for 288, 305, 306, 321,
281,
Sustainability 2024, and
16, x FOR 285.
PEER This means that 85% of the censuses are grouped within the9 censuses
REVIEW of 19 from
the same population. NP El Palmar and Gualeguaychú show a lower distance explained
by vegetation composition.

Sustainability 2024, 16, x FOR PEER REVIEW 9 of 19

Figuredendrogram.
Figure 7. Cluster 7. Cluster dendrogram.
K = 3.KThe= 3. The colorsindicate
colors indicate the grouping
the of the of
grouping censuses into the three
the censuses into the three
main groups. The colors of the numbers represent different censuses of the same population.
main groups. The colors of the numbers represent different censuses of the same population.

Consistent with the cluster analysis, the representation of the two principal coordinates
in the PCoA (Figure 8) shows a clustering of censuses from the same locality, except for 288.
In other words, the clustering into three main groups predominantly includes censuses from
the same populations. Principal coordinates explain the 22.5 and 14.2% of the variation.
Also, in the populations of NP El Palmar and Gualeguaychú, a greater dispersion is
observed in the multidimensional scaling compared to Concordia, which appears to have a
more homogeneous vegetation composition. The MRPP analysis of species composition
changes showed significant
Figure 7. Cluster dendrogram.differences among
K = 3. The colors indicate the sampled
the grouping of the censusespopulations
into the three (delta = 0.001).
main groups. The colors of the numbers represent different censuses of the same population.

Figure 8. Principal Coordinate Analysis (PCoA) of associated woody and semi-woody species of
Hexachlamys edulis populations. Each point represents a unique individual or census, colored according
Sustainability 2024, 16, x FOR PEER REVIEW 10 of 19
Sustainability 2024, 16, 10029 9 of 17

Figure 8. Principal Coordinate Analysis (PCoA) of associated woody and semi-woody species of
Hexachlamys edulis populations. Each point represents a unique individual or census, colored ac-
to its population
cording of origin:ofConcordia
to its population (red), NP(red),
origin: Concordia El Palmar
NP El (yellow), and Gualeguaychú
Palmar (yellow), (green).
and Gualeguaychú
(green). Ellipses indicate the variability within each population. The x-axis (Principal Coordinate
Ellipses indicate the variability within each population. The x-axis (Principal Coordinate 1) and 1)
and y-axis (Principal Coordinate 2) represent the axes of variation, explaining 25.4% and 14.9% of
y-axis (Principal Coordinate 2) represent the axes of variation, explaining 25.4% and 14.9% of the total
the total variance,
variance, respectively.
respectively.

the discriminant
In the discriminantanalysis,
analysis,the
themaximum
maximumseparation
separation between
between groups
groups andand
thethe rela-
relative
tive location of the species represented in the discriminant canonical axes can
location of the species represented in the discriminant canonical axes can be observed be observed
(Figure 9). The separation between groups is complete, and the apparent error rate from
cross-validation waswas 0%.
0%.This
Thisvalidation
validation implies that
implies if some
that datadata
if some are are
obtained fromfrom
obtained one
one of these
of these populations
populations without
without knowing
knowing whichwhich
one, one,
and and we represent
we represent its position
its position in
in this
this multidimensional
multidimensional space,
space, we would
we would correctly
correctly identify
identify the population
the population with awith a success
success prob-
probability of 100%.
ability of 100%.

Figure 9. Discriminant Analysis of associated woody and semi-woody species of Hexachlamys edulis
populations. Each
populations. Eachpoint
pointrepresents
represents a unique
a unique individual,
individual, colored
colored according
according to its to its population
population of
of origin:
origin: Concordia (red), El Palmar (yellow), and Gualeguaychú (green). The canonical
Concordia (red), El Palmar (yellow), and Gualeguaychú (green). The canonical axes represent the axes repre-
sent the
linear linear combinations
combinations of ecological
of ecological variables
variables that
that best best discriminate
discriminate between
between the populations.
the populations. The
The closer the points of a given population are to each other, the more similar they are in terms of
closer the points of a given population are to each other, the more similar they are in terms of their
their ecological characteristics.
ecological characteristics.
Sustainability 2024, 16, 10029 10 of 17

4. Discussion
4.1. Relationships Among Biodiversity Indicators and Populations
The consistency in species diversity among the studied locations, as observed in
this study and supported by Oliveira–Filho’s research [33], underscores the reliability
of the obtained results. Concordia exhibits a high species richness with 75 registered
species, albeit with a moderate coincidence rate of 31.4%. On the other hand, NP El
Palmar displays a richness of 71 species, with a relatively higher coincidence rate of 34.3%.
Gualeguaychú, while having a lower species richness with 60 species, still maintains a
noteworthy coincidence rate of 33.3%. Hence, a considerable number of species and families
associated with H. edulis have been successfully recorded in the studied populations. While
in terms of alpha diversity, the obtained results and the compared literature seem quite
disparate, it should be noted that the bibliographic source consists of a multi-year project
that draws from many other sources, which could explain the lower number of species
in this study. However, this information allows us to assert that the degree of species
representativeness among sites is, at the very least, similar.
In general, regarding richness, abundance, the Shannon index, and dominance, less
favorable conditions are observed in NP El Palmar compared to Gualeguaychú. The lowest
values of richness and abundance recorded in NP El Palmar may be attributed to the
majority of H. edulis trees being isolated and located outside areas of dense vegetation.
As stated by Micou [34], in the riparian areas with dense and closed vegetation and a
significant presence of Ligustrum lucidum, which is considered an invasive species and a
threat to the conservation of regional biodiversity, H. edulis trees were not found. These
reasons might lead to the assumption that H. edulis is, in turn, adapted to specific stands
within the landscape’s heterogeneity.
Overall, it is suggested that for the three sites, there is a group of species that are
relatively dominant in each community, while others have a less pronounced presence. This
indicates a non-uniform distribution of species abundance, but the value is not extremely
high, which could be considered moderately positive in terms of biodiversity. The higher
dominance in NP El Palmar could be explained due to many species being surveyed only
once, while a few species were recorded more frequently, such as Solanum mauritianum (26),
Scutia buxifolia (17), and Myrrhinium atropurpureum (14). Solanum mauritianum (38) and
Asparagus setaceus (31) were two markedly dominant species in Gualeguaychú, while only
three species were recorded once. The same trend was observed with Pielou equitability,
although no differences were found.
While the Shannon index has significant differences between NP El Palmar and
Gualeguaychú, we cannot strictly conclude differences in site biodiversity based on this in-
dicator, as it measures entropy and the state of the complexity rather than biodiversity [35].
In other words, we could conclude that there is greater biological complexity, but not neces-
sarily greater diversity per se in Gualeguaychú compared to NP El Palmar. Furthermore, the
indicators that measure biodiversity more strictly, such as evenness and Margalef, showed
that there are no conclusive differences between the sites where H. edulis grows. Broadly
speaking, the values of biodiversity indicators might seem not very encouraging, but it
should be kept in mind that the surveys were only restricted to woody and semi-woody
species, the precipitation and average temperature regime corresponds to a subtropical to
temperate transition zone, and it is known that these climatic variables are correlated with
the quantity of species and individuals [36]. It should also be considered that comparative
differences with other studies could be due to the fact that the surveys were based on
species associated with a single species.

4.2. Impact of Human Activity on Native and Exotic Species Dynamics

The relationships between native and exotic species provide insight into the impact
of human activity. The anthropic indicator shows Gualeguaychú has the lowest native-
to-exotic species ratio, suggesting higher anthropization. While biodiversity indicators
may appear favorable, they often include exotic species that disrupt the original ecological
Sustainability 2024, 16, 10029 11 of 17

balance. Introductions of non-native trees and shrubs have caused invasive species to
spread, negatively impacting ecosystems globally [37]. In Gualeguaychú, despite limited
public access, the lower ratio (0.70) suggests that nearby forestry activities contribute to
the establishment of non-native species. In contrast, NP El Palmar, despite tourism and
recreational use, maintains a higher proportion of native species (0.78), likely due to its
conservation status. Concordia, with the highest anthropic indicator value (0.85), seems
less impacted by exotic species despite surrounding recreational activities.
These findings highlight the complex ways human activities influence local biodiver-
sity. Even minor disturbances can significantly shift species composition, as the introduc-
tion of exotic species often leads to the displacement of native flora, affecting ecosystem
functions and resilience. Managing the introduction of non-native species and closely
monitoring their impact should be central to conservation efforts.

4.3. Vegetation Community Dynamics and Multivariate Analysis

Also, it is demonstrated that individuals of H. edulis are found in different vegetation
communities of the riparian forest of the Uruguay River and are adapted to different
conditions of biodiversity, competition, and environment in terms of accompanying woody
and semi-woody species. Other studies have successfully set a precedent for combining
PCoA with Hierarchical Cluster Analysis [38], as they perform a hierarchical clustering of
the observations and then represent them in an ordination obtained with PCoA using the
same distance measure used in the clustering, for example, as conducted by Ulloa et al. [39].
Other studies have even confirmed differences in the composition of tree vegetation in the
gallery forests of the Uruguay River according to climatic, physiographic, and edaphic
environment [23,40]. In the Cluster Analysis, NP El Palmar and Gualeguaychú show a
lower distance explained by vegetation composition. The similarities could be explained by
the species Solanum mauritianum, Scutia buxifolia, Schinus longifolius, and Fuchsia magellanica
being present in all three sites. The three statistical analysis tools, i.e., cluster analysis, PCoA,
and discriminant analysis, complement each other and consistently demonstrate that the
plant communities where H. edulis spontaneously grows are different, and the composition
of vegetation among populations is heterogeneous. Additionally, as shown by Cluster
Analysis, a closer similarity is observed between El Palmar and Gualeguaychú, which
could be explained by a greater difference in annual average temperature and precipitation
compared to Concordia.

4.4. Native Species for Enhancing Biodiversity in Cropping Systems

Some registered native species worth highlighting for possible incorporation into
farming systems to improve biodiversity are Allophylus edulis, Butia yatay, Eugenia uniflora,
Eugenia uruguayensis, and Muehlenbeckia sagittifolia. Allophylus edulis, commonly known as
“chal-chal,” is a small tree or shrub with edible fruits rich in antioxidants and medicinal
properties, traditionally used for gastrointestinal disorders and inflammation [41,42]. Butia
yatay, or “yatay palm,” produces nutritious edible dates that can be transformed into
value-added products and serves as a vital nectar source for honey production while
providing habitat for wildlife [43,44]. Eugenia uniflora, known as “Surinam cherry” or
“pitanga,” offers delicious sweet-tart fruits and has been used traditionally for digestive
issues and respiratory problems; it also shows promise in breeding programs and contains
bioactive essential oils [45–48]. Eugenia uruguayensis possesses antimicrobial and anti-
inflammatory properties due to its leaf oil compounds [49], making it a profitable alternative
for agricultural production [50]. Lastly, Muehlenbeckia sagittifolia, or “wire vine,” is a
hardy climbing plant with small, edible fruits and multiple uses in erosion control and
landscaping [51].
Incorporating these native species into agroforestry practices can enhance biodiversity,
provide economic opportunities, and support sustainable agricultural practices. Future
studies should explore their full potential and develop best practices for their cultivation
Sustainability 2024, 16, 10029 12 of 17

and use. While these five species have been highlighted for their particular potential, it is
important to note that other species found in these sites likely also possess valuable uses.

5. Conclusions
This study successfully recorded a considerable number of species and families associ-
ated with H. edulis in the studied populations indicating a diverse plant community within
the habitat of H. edulis.
Biodiversity indicators, including richness, the Shannon index, and dominance re-
vealed variations among the studied sites. These indicators provide insights into the
ecological complexity and community structure within each population.
The anthropic indicator highlighted the impact of human activity, with differences in
the ratio of native-to-exotic species among the populations, suggesting varying degrees of
human influence and potential conservation challenges.
Statistical multivariate analyses, such as cluster analysis, PCoA, and discriminant anal-
ysis, consistently demonstrated differences in plant communities among the populations.
These variations reflect the heterogeneity of the landscape and the adaptability of H. edulis
to different ecological conditions and associated species.
The results of this study not only contribute to the sustainable management of
H. edulis, but also have broader implications for enhancing agroforestry practices with
similar species. Among the species grown along with H. edulis, this study successfully iden-
tified five promising native plant species for agroforestry applications: Allophylus edulis,
Butia yatay, Eugenia uniflora, Eugenia uruguayensis, and Muehlenbeckia sagittifolia. These
species offer a wealth of benefits including edible fruits, medicinal properties, ecological
advantages for biodiversity and bioremediation, economic opportunities through fruit
production and handicrafts, and support for sustainable agricultural practices.
Results obtained can serve as baseline information for future research on the dy-
namics of vegetation in these areas and on the studied H. edulis species. Finally, these
findings contribute to understanding how wild species like H. edulis adapt to different plant
communities, which might be valuable for developing new agroecological approaches or
identifying potential companion planting species in future agricultural systems.

Author Contributions: Conceptualization, I.S.P., M.E.A., and S.R.; methodology, I.S.P., M.E.A., and
M.A.; software, I.S.P.; validation, I.S.P. and M.A.; formal analysis, I.S.P. and S.R.; investigation, I.S.P.,
M.E.A., and S.R.; resources, I.S.P. and M.E.A.; data curation, I.S.P., M.A., and S.R.; writing—original
draft, I.S.P.; writing—review and editing, I.S.P., M.E.A., M.A., and S.R.; visualization, I.S.P. and S.R.;
supervision, I.S.P., M.E.A., and S.R.; project administration, M.E.A. and S.R. All authors have read
and agreed to the published version of the manuscript.
Funding: This work was supported by the University of Morón [PICTO-UM-2019-00003] and CON-
ICET [PIP 11220200102292CO].
Institutional Review Board Statement: Not applicable.
Informed Consent Statement: Not applicable.
Data Availability Statement: The data supporting the results of this study are available at https:
//github.com/ipovilonis/ipovilonis.github.io/blob/main/II_ER_Asociatedspecies.Rmd (accessed
on 13 November 2024) and can be accessed publicly.
Acknowledgments: We would like to especially thank Susana Luisa Stoffella for her contributions.
We appreciate the collaboration of INTA Concordia, Establecimiento Pampa Azul, the National Park
El Palmar, and El Potrero de San Lorenzo reserve.
Conflicts of Interest: The authors declare no conflicts of interest.
Sustainability 2024, 16, 10029 13 of 17

Appendix A

Table A1. Presence (P) and absence (A) of native and exotic species and abundance in Concordia, NP
El Palmar, and Gualeguaychú. The complementary figure below shows the species found at each site
and their abundance.

Family Species Concordia NP El Palmar Gualeguaychú

Native
FABACEAE Acacia caven P P P
SAPINDACEAE Allophylus edulis P P P
LILIACEAE Asparagus setaceus A A P
FABACEAE Bauhinia forficata A A P
MYRTACEAE Blepharocalyx salicifolius P P A
LOGANIACEAE Buddleja globosa A A P
ARECACEAE Butia yatay P P A
ULMACEAE Celtis iguanaea A A P
ULMACEAE Celtis tala P P P
RUBIACEAE Cephalanthus glabrotus P A A
SOLANACEAE Cestrum parqui A A P
VITACEAE Cissus verticilata P A A
RUTACEAE Citrus aurantium A P A
RANUNCULACEAE Clematis montevidensis P A A
CUCURBITACEAE Cyclanthera hystrix P A A
BIGNONIACEAE Dolichandra cynanchoides A P A
FABACEAE Erythrina crista galli P A P
MYRTACEAE Eugenia uniflora P A P
MYRTACEAE Eugenia uruguayensis P P P
ENOTERACEAE Fuchsia magellanica A P P
ASTERACEAE Heterothalamus alienus P A A
MYRTACEAE Hexachlamys edulis A A P
BIGNONIACEAE Jacaranda mimosifolia A P A
TILIACEAE Luehea divaricata P A A
BIGNONIACEAE Magfadenia unguis cati A P A
CELASTRACEAE Maytenus ilicifolius A A P
POLYPODIACEAE Microgramma lycopodioides A P A
FABACEAE Mimosa pilulifera P A A
FABACEAE Mimosa sp. P A A
POLYGONACEAE Muehlenbeckia sagittifolia P A P
MYRTACEAE Myrrhinium atropurpureum A P A
MYRSINACEAE Myrsine laetevirens A A P
MYRTACEAE Myrtus mucronatum P A A
LAURACEAE Ocotea acutifolia P A A
Sustainability 2024, 16, 10029 14 of 17

Table A1. Cont.

Family Species Concordia NP El Palmar Gualeguaychú

MALVACEAE Pavonia malvacea P A A
FABACEAE Poecilanthe parviflora P A A
SAPOTACEAE Pouteria salicifolia A P P
EUPHORBIACEAE Sapium haematospermun A P A
ANACARDIACEAE Schinus longifolius A P P
ANACARDIACEAE Schinus molle A P A
RHAMNACEAE Scutia buxifolia A P P
EUPHORBIACEAE Sebastiania brasiliensis P A P
FABACEAE Sesbania punicea P A A
SOLANACEAE Solanum amygdalifolium P A A
SOLANACEAE Solanum jazminoides A P A
SOLANACEAE Solanum mauritianum A P P
MALPIGHIACEAE Stigmaphyllon bonarense P A A
COMBRETACEAS Terminalia australis P A A
ASTERACEAE Tessaria integrifolia P A A
VERBENACEAE Verbena littoralis A P A
Exotic
VERBENACEAE Aloysia gratissima A P A
BASELLACEAE Anredera cordifolia P A A
VERBENACEAE Citharexylum montevidense P A A
ROSACEAE Crataegus oxyacantha A P A
EPHEDRACEAE Ephedra twediana A P P
MYRTACEAE Eucalyptus grandis P A A
PROTEACEAE Grevillea robusta A P A
CONVOLVULACEAE Ipomea sp. P A A
CONVOLVULACEAE Ipomoea cairica P P A
OLEACEAE Jazminum humile A P A
JUNCACEAE Juncus acutus P A P
VERBENACEAE Lantana camara A A P
OLEACEAE Ligustrum lucidum A P A
OLEACEAE Ligustrum sinensis A P A
MELIACEAE Melia azederach A P A
MALVACEAE Pavonia hastata P A A
LAURACEAE Persea americana A A P
ARECACEAE Phoenix canariensis P A A
SALICACEAE Populus nigra A A P
SALICACEAE Salix babylonica A P A
Total 35 32 26
 MALVACEAE Pavonia hastata P A A
LAURACEAE Persea americana A A P
ARECACEAE Phoenix canariensis P A A
SALICACEAE Populus nigra A A P
Sustainability 2024, 16, 10029 SALICACEAE Salix babylonica A P A15 of 17
Total 35 32 26

Figure A1. The figure is complementary to Table 1.

The figure is complementary to table 1
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