Article

Establishment and Natural Regeneration of Native Trees in

Agroforestry Systems in the Paraguayan Atlantic Forest
Amado Insfrán Ortiz 1,2, * , José María Rey Benayas 2 and Luis Cayuela 3

1 Faculty of Agrarian Sciences, National University of Asunción, San Lorenzo University Campus, km 10,
Asunción 1618, Paraguay
2 Forest Ecology and Restoration (FORECO) Group, Life Sciences Department, University of Alcalá,
28871 Alcalá de Henares, Madrid, Spain
3 Department of Biology and Geology, Physics and Inorganic Chemistry, Rey Juan Carlos University, c/Tulipán s/n,
28933 Móstoles, Madrid, Spain
* Correspondence: amado.insfran@agr.una.py

Abstract: The establishment of planted trees and the natural regeneration of trees in agroecosystems
is challenging. This study evaluated the establishment and natural regeneration of the following
six native tree species in two agricultural systems in the Atlantic Forest in Paraguay: Cedrela fissilis
Vell., Cordia trichotoma (Vell) Arráb. ex Steud., Handroanthus albus (Cham.) Mattos, Handroanthus
impetiginosus (Mart. ex DC.) Mattos, Peltophorum dubium (Sprengel) Taubert, and Cordia americana
(L.) Gottschling and J.S.Mill. At the study site in Caaguazú, 18 plots of 100 m2 each were established
in 2 agronomic systems (conventional or agroecological) featuring 3 plantation types (pathsides,
agricultural field edges, and islets). Trees were planted at this site in spring 2010 at a density
of 1800 individuals ha−1 , and the site was monitored for six years. At the study site in Itapúa,
30 plots of 50 m2 each were established in three agronomic systems (conventional, traditional, or
agroecological). Trees were planted at this site in spring 2012 at a density of 1600 individuals ha−1 ,
Citation: Insfrán Ortiz, A.; Rey
and the site was monitored for four years. Survival and relative growth rates of the planted species
Benayas, J.M.; Cayuela, L. and natural regeneration were analyzed using generalized linear mixed models that considered
Establishment and Natural species, agronomic system, and plantation type as fixed factors, and time and plot as random factors.
Regeneration of Native Trees in At both sites, survival varied among species. Here, C. fissilis showed lower survival and C. trichotoma
Agroforestry Systems in the higher growth than the other species. Naturally regenerated species were C. trichotoma, H. albus,
Paraguayan Atlantic Forest. Forests and P. dubium. The agronomic system and species affected growth and natural regeneration at both
2022, 13, 2045. https://doi.org/ locations. Plantation type affected survival and growth in Caaguazú only. We conclude that species
10.3390/f13122045
contributes more than agronomic system or plantation type to determining the survival, relative
Academic Editor: Mark S. Ashton growth rate, and natural regeneration in agroforestry systems in the Paraguayan Atlantic Forest.

Received: 20 October 2022

Keywords: agroecosystem; agroecology; growth; recruitment; subtropical; survival
Accepted: 21 November 2022
Published: 1 December 2022

Publisher’s Note: MDPI stays neutral

with regard to jurisdictional claims in 1. Introduction
published maps and institutional affil-
Reduction in forest areas, mainly because of the expansion of agriculture [1,2], causes
iations.
the loss of biodiversity and habitats and affects the provision of ecosystem services [3–5].
In tropical and subtropical countries, agricultural expansion is responsible for 73% of
deforestation [6] and is a leading cause of species decline, including 74% of threatened
Copyright: © 2022 by the authors.
bird species [7]. This has reduced the provision of ecosystem services, particularly those
Licensee MDPI, Basel, Switzerland. with regulatory functions, such as soil retention, runoff control, and nutrient cycles [8].
This article is an open access article The Atlantic Forest in Paraguay has been severely affected by large-scale habitat loss and
distributed under the terms and fragmentation [9].
conditions of the Creative Commons One way to counteract the harmful effects of agriculture is establishing and maintain-
Attribution (CC BY) license (https:// ing agroforestry systems, where wildlife-friendly farming that allows more sustainable
creativecommons.org/licenses/by/ agricultural land use is practiced [10,11]. Agroforestry systems deliberately combine
4.0/). trees and shrubs with some crops [12], leading to levels of biodiversity and ecosystem

Forests 2022, 13, 2045. https://doi.org/10.3390/f13122045 https://www.mdpi.com/journal/forests

Forests 2022, 13, 2045 2 of 15

services intermediate between those in agricultural areas without trees and those of na-
tive forests [13,14]. Thus, the combination of native tree species with agricultural crops
is a valuable strategy that integrates agricultural production and biodiversity conserva-
tion [3,11,15,16]. Unfortunately, this strategy still faces economic obstacles and so has not
been widely applied [11,17].
Trees can be planted in agricultural landscapes as linear elements, such as living
fences, on the edges of agricultural fields, pathsides, and banks [10,18] and as islets, thereby
minimizing competition for agricultural space [19]. Both strategies provide a variety of
environmental goods and services [20], such as the maintenance and improvement of
biodiversity [13], including pollinators and enemies of natural pests [21], the regulation
of runoff and sediment and nutrient retention [1], water infiltration [22], production of
edaphic organic matter [23,24], microclimate regulation [25], landscape connectivity [18],
scenic beauty [26], and crop productivity [1]. In addition, agroforestry systems can provide
benefits that help reduce pressure on the remaining forests [27]. For example, planted trees
can export seeds and nucleate the growth of other shrub and tree species, constituting a sys-
tem straddling between a naturally regenerated forest and a forest plantation. They allow
large-scale passive reforestation, where vegetation and soil can sequester carbon [19,28].
The establishment of native trees in tropical and subtropical agroecosystems, whether
in plantations or as part of natural regeneration, depends mainly on the species, manage-
ment after forest plantation, and type of agroecosystem [29,30]. Such species are often
planted in sections of agricultural fields or in cattle grazing areas [31,32]. In agricultural
landscapes, native trees can be established along pathsides, the edges of agricultural fields,
and in islets [33], which are forms of nucleation [34]. However, the factors affecting the
success of these efforts at plantation and natural regeneration sites are unclear.
Thus, the objective of the present study was to evaluate the establishment (survival
and growth) and natural regeneration of native tree species planted in linear form (path-
sides and field edges) or islets (Figure S1) in conventional, traditional, or agroecological
agricultural systems in the Atlantic Forest in Paraguay. The differences between these
systems are indicated in Table S1. For this purpose, experimental plantations were mon-
itored for 4–6 years. Our hypotheses were that tree survival, growth, and regeneration
would depend on the following: (1) the species planted; (2) the agronomic system, with
agroecological systems being the most favorable for the establishment and natural regener-
ation of planted trees because of the high soil quality and absence of pesticides; and (3) the
type of plantation, with islets providing the best establishment and natural regeneration
because they are less exposed to sun, livestock, and wind. The results of this work may
help guide the transformation and conversion of conventional treeless agroecosystems into
more sustainable agroforestry systems in the Neotropics.

2. Materials and Methods

2.1. Study Area
The study was conducted in the municipalities of Repatriación (Department of Caaguazú)
and of Carlos Antonio López (Department of Itapúa) in the Atlantic Forest of Paraguay
(Figure 1).
The climate in this area is characteristic of the semi-deciduous subtropical Atlantic
Forest, with frequent rains totaling 1300–1800 mm/year and an average annual temperature
of 22 ◦ C, with a minimum of 0 ◦ C (winter) and a maximum of 42 ◦ C (summer) [36]. The
soil in the two areas differs. In the plantation area in Caaguazú, the soil is of sandstone
origin and belongs to the Ultisol order and arenic rhodic paleudult sub-group (classes III
and IV) in the sand-clay textural subdivision containing 20%–30% of clay and showing
strong water erosion and high degradation [37]. In the plantation area in Itapúa, the soil is
of basaltic origin and belongs to the Ultisol order and rhodic paleudult subgroup (class II)
in the fine clay textural subdivision containing 30%–40% of clay and showing moderate
water erosion and medium-level degradation [37]. The main economic activities in the
two areas are agriculture, mostly the cultivation of cotton, corn, sugarcane, beans, yerba
 Forests 2022, 13, 2045 3 of 15

R REVIEW 3 of 16
mate, cassava, wheat, and soybean, with a predominance of monocultures in conventional
systems; and the rearing of cattle, pigs, and poultry [38].

Figure
Figure 1. Identification of the 1. Identification
study area (a)ofinthe
thestudy area (a) in and
Neotropics the Neotropics
(b) in theand (b) in the
eastern eastern
region ofregion
Para-of
Paraguay, and location of the experimental plantations in (c) Caaguazú and (d) Itapúa. Panels a and
guay, and location of the experimental plantations in (c) Caaguazú and (d) Itapúa. Panels a and b
b show the distribution area of the Atlantic Forest according to [35].
show the distribution area of the Atlantic Forest according to [35].

The climate in this area is characteristic of the semi-deciduous subtropical Atlantic

Forest, with frequent rains totaling 1300–1800 mm/year and an average annual tempera-
Forests 2022, 13, 2045 4 of 15

The Atlantic Forest, one of the most biodiverse biomes in the world, is also one of
the most threatened [39]. It occupies an estimated area of 8,500,000 ha in Paraguay [40],
accounting for 55% of the country’s eastern region [36]. Most of this native forest was intact
in 1940 [41], and the intact proportion fell to 73.4% by 1973 and to 24.9% by 2000 [42], and
it stands now between 10 and 13% [43]. The main drivers of forest loss and degradation
in this region are large-scale agriculture [44], mainly the cultivation of soybean [45], small
landowner settlements, and the extraction of high-value timber species, such as Amburana
cearensis (Allemão) SCSm., Cedrela fissilis, and Myrocarpus frondosus Fr. Allem [46].

2.2. Experimental Description

The study included two departments (Caaguazú and Itapúa), three agronomic sys-
tems (conventional, traditional, and agroecological), and three plantation types (linear on
pathsides, edges of agricultural fields, and islets; Table 1).

Table 1. Experimental plantations established at the study sites.

Agronomic Tree Density Monitoring

Location Plantation Type No. Plots Plot Size (m2 )
System (Individuals ha−1 ) Period (Years) *
Conventional Pathside 3 100 1800 2010–2016
Field edge 3 100 1800 2010–2016
Islet 3 100 1800 2010–2016
Caaguazú Agroecological Pathside 3 100 1800 2010–2016
Field edge 3 100 1800 2010–2016
Islet 3 100 1800 2010–2016
Total 18
Conventional Islet 10 50 1600 2012–2016
Traditional Islet 10 50 1600 2012–2016
Itapúa Agroecological Islet 10 50 1600 2012–2016
Total 30
* Years monitored are as follows: 2010, 2012, 2014, and 2016. The monitoring of survival, growth, and natural
regeneration was carried out from the first year of establishment of the plots (month of December).

The conventional agronomic system primarily includes large plots (>50 ha) where
high-yield seed varieties [47] are cultivated using large amounts of agrochemicals [48,49]
and mechanization; the production is mainly for export [50]. The traditional system, in con-
trast, is practiced by small farmers (plots < 20 ha) [49], who in Paraguay are mainly family
farmers who cultivate plots < 10 ha [51]. Traditional agriculture is based on technological,
cultural, and local knowledge practices, diversified crops [52], and minimal mechaniza-
tion [53]. The agroecological system is practiced by small farmers [54] and is based on
farmers’ knowledge, ecological principles, cultivated and uncultivated biodiversity [55],
resistant and resilient systems, energy efficiency, and social justice [56]. In this system,
pest management, nutrient cycles, biomass recycling, biological interactions, and biodiver-
sity synergies are leveraged to promote ecosystem services, agricultural production, and
biodiversity conservation [57,58].
In Caaguazú, tree plantations were established on two farms. The two farms were
similar in terms of soil conditions, terrain, elevation, and climate, in order to minimize
potential confounding effects between farm and agroecological system. However, the
farm management is different. One was managed according to conventional practices
(coordinates 25◦ 340 37.3000 S and 55◦ 450 01.5300 W, average altitude of 270 m above sea
level), and the other according to agroecological practices (coordinates 25◦ 330 11.2500 S and
55◦ 550 38.0200 W, average altitude of 325 m above sea level), Table S1. The three types of
tree plantation were established in each farm/agronomic system, including three plots
of 100 m2 each for each plantation type. Plot dimensions were 10 m × 10 m in the case
of pathsides and islets, or 2.5 m × 40 m in the case of agricultural field edges (Table 1).
Forests 2022, 13, 2045 5 of 15

Six native tree species were planted in October 2010, as follows: H. albus, H. impetigi-
nosus, P. dubium, C. fissilis, C. trichotoma (a tree species valued for wood furniture), and
C. americana (valued for rural buildings, firewood, and poles). All these species occupy
the arboreal stratum (20–30 m high) of the Atlantic Forest in Paraguay. Ilex paraguariensis
Saint Hilaire (yerba mate) was also planted and shares the space as an economically im-
portant annual cut crop, but it was excluded from this study. The planting density of the
native species was 1800 individuals ha−1 (18 individuals/plot), and that of I. paraguariensis
was 500 individuals ha−1 (5 individuals/plot), with an average distance of 2.5 m between
plants (Figures S1 and S2). The individuals were planted at a depth of 20 cm and irri-
gated at 30 L m−2 during the first year after planting to help them withstand the first
summer drought.
In Itapúa, plantations were established on a farm that was managed traditionally
(coordinates 26◦ 240 56.8700 S and 54◦ 450 33.5700 W, average altitude of 209 m above sea level).
Thirty experimental plantation plots were established only as islets in the three agronomic
management systems. Each system included 10 plots of 2.5 m × 20 m (Table 1). Plantations
were established in October 2012 using five native tree species, i.e., the same as in Caaguazú
except for C. americana, which was unavailable in nurseries. The species were planted
at a density of 1600 individuals ha−1 (8 individuals/plot), together with I. paraguariensis
(2600 individuals ha−1 , 13 individuals/plot). The plantations were established after a
precipitation of 40 L m−2 . The spatial arrangement was “staggered”, with 2 m between
plants in the same row and 2.5 m between rows. The planting depth was 15 cm (Figure S3).
The differences between the two sites in planting density, planting depth, and watering
reflected the fact that the sandy soil in Caaguazú was looser and retained less water than
the basaltic soil in Itapúa. Plantation management also differed between the two locations
in terms of soil tillage, fertilizer, I. paraguarienses crop density, and annual practices to
control weeds and harmful insects (Table S1). The initial average heights of the planted
seedlings are reported in Table S2.

2.3. Monitoring the Establishment and Natural Regeneration of Tree Species

Survival of planted individuals was monitored in spring (October and November)
in the years 2012, 2014, and 2016 in Caaguazú, and the years 2014 and 2016 in Itapúa.
The number of surviving or dead individuals and the apparent causes of mortality were
recorded at all plantation plots. Simultaneously, the numbers of individuals of the different
species that were established through natural regeneration were recorded. Tree height (x)
was measured to estimate the relative growth rate in October and November, which was
calculated as follows:
[ln(x) at the last measurement − ln(x) at the first measurement]/total no. of days.

2.4. Data Analysis

We applied generalized linear mixed models to study the effect of the species planted,
the agronomic system, and the type of plantation on survival, growth, and natural regen-
eration of seedlings over time at the two locations. In Itapúa, as there was only one form
of plantation (islet), this effect was not studied. We used different error distributions for
each response variable, as follows: binomial for survival (proportion data), gamma for
growth (continuous data), and Poisson for natural regeneration (count data). The complete
model incorporated the species, agronomic system, and plantation type as fixed factors,
and the sampling year as a covariate, including all possible pairwise interactions among
these predictor variables and the triple interaction among species, agronomic system, and
plantation type. Plot was included as a random factor.
All possible sub-models were compared using the Akaike information criterion cor-
rected for small sample sizes (AICc), and models with ∆AICc ≤ 2 with respect to the best
model were selected [59]. In cases with more than one ‘best model’, the most complex
model was selected. The residuals of the best model(s) were explored using a simulation-
based approach [60]. Multiple post-hoc comparisons were conducted using Tukey tests,
Forests 2022, 13, 2045 6 of 15

with a significance level of 0.05, to determine the effects of different combinations of agro-
nomic systems and plantation types on each of the response variables for each of the
study species.
All analyses were performed with R [61] using the packages ‘lme4’ [62], ‘MuMIn’ [63],
‘multcomp’ [64], and ‘DHARMA’ [65].

3. Results
3.1. Survival of Planted Species
In Caaguazú, comparison of models with ∆AICc ≤ 2 indicated that the planted species,
agronomic system, and plantation type influenced survival probability (Tables 2 and S3a).
At six years after planting, the studied species showed different average survival rates
independently of other factors; C. fissilis showed the lowest survival rate (33.3 ± 34.3%) and
C. americana the highest (91.7 ± 19.2%; Table S4a). Plantations in the agroecological system
had higher survival rates (69.1 ± 14.8%) than in the conventional system (57.4 ± 24.3%).
The higher survival in agroecological systems depended on (1) the type of plantation,
with higher survival on pathsides and agricultural field edges, and (2) the species, with
agroecological systems favoring the survival of C. fissilis, P. dubium, and H. impetiginosus
more than the survival of H. albus, C. trichotoma, and C. americana. The effect of the
agronomic system was not observed for the species as a whole (Figure 2).

Table 2. Plausible models for the survival of planted species in the two agroforestry experiments.

Site Model (Intercept) AICc Delta Weight R2 m R2 c

Caaguazú 512 3,590,128 959.8110 0.0000000 269,608.5 0.8687040 0.8748712
1024 3,750,841 960.4830 0.6720045 192,668.1 0.8671280 0.8733760
384 3,656,629 961.1081 1.2971396 140,949.4 0.8633484 0.8693383
Itapúa 24 0.5699077 556.5128 0.000000 863,392.6 0.2894882 0.2924227
Abbreviations are as follows: AICc, Akaike information criterion corrected for ∆AICc ≤ 2; R2 c, conditional R2
indicating the variability explained by the fixed and random effects; R2 m, marginal R2 that considers only the
variability explained by the fixed effects.

In Itapúa, the comparison of models with ∆AICc ≤ 2 showed a significant effect of

species and agronomic system on probability of survival (Tables 2 and S3a). The five species
analyzed had different average survival rates (Figure 2 and Table S4a). Again, C. fissilis
had the lowest survival rate (33.3 ± 47.9%), while C. trichotoma had the highest survival
(75.00 ± 36.55%). The agronomic system did not significantly affect the survival of C. fissilis
or H. albus, in contrast to the rest of the species (Figure 2 and Table S4a).

3.2. Growth of Planted Species

Comparison of models for Caaguazú indicated that the species, agronomic system,
and plantation type influenced the growth rate of individuals. In Itapúa, however, only the
species had a significant influence (Table 3). The species differed in their relative growth
rates after 2212 days since planting in Caaguazú and after 1425 days in Itapúa (Figure 3a,b
and Table S4b). At both sites, C. trichotoma showed higher relative growth than the other
species (Figure 3). The agronomic system affected the relative growth rate in Caaguazú,
being higher in the conventional system (0.00144 ± 0.00066 m day−1 ) than in the agroecolog-
ical system (0.00139 ± 0.000234 m day−1 , p ≤ 0.01), but this was not observed in Itapúa (con-
ventional at 0.00211 ± 0.000108 m day−1 , agroecological at 0.00214 ± 0.000096 m day−1 ,
and traditional at 0.00213 ± 0.000159 m day−1 ) (Figure 3a,b and Table S4b). The relative
growth rates in Caaguazú differed across the different plantation types in the following
order (Figure 3c and Table S4b): field edges (0.00149 ± 0.000203 m day−1 ) > pathsides
(0.00147 ± 0.000257 m day−1 ) > islets (0.00136 ± 0.000265 m day−1 ).
 Forests 2022, 13, 2045 7 of 15

Table 3. Plausible models for the growth of the planted species in the two agroforestry experiments.

Site Model (Intercept) AICc Delta Weight R2 m R2 c

Caaguazú 40 6,978,656 298.5042 0.000000 946,708.8 0.8671280 0.8733760
Itapúa 2 0.2708572 638.4951 0.000000 888,152.8 0.2894882 0.2924227
Forests 2021, 12, x FOR PEER REVIEW 7 of
Abbreviations are as follows: AICc, Akaike information criterion corrected for a ∆AICc ≤ 2;R2 c: conditional R2
indicating the variability explained by the fixed and random effects; R2 m, marginal R2 that considers only the
variability explained by the fixed effects.

Figure 2. Survival of the planted species in different agronomic systems and plantation types. The
Figure
time 2. Survival
interval of the
in Caaguazú andplanted
in Itapúaspecies
was fromin different agronomic
2010 to 2016 and fromsystems and respectively.
2012 to 2016, plantation types. T
time
The interval(a–f)
subfigures in Caaguazú and inThe
are the species. Itapúa was
letters from
“a”, “b”,2010 to 2016
“c”, “ab”, and“A”,
“bc”, from“B”2012
andto“AB”,
2016,are
respective
The subfigures
statistical (a–f)
differences andare the species.
similarities The letters
between "a", "b",
agricultural "c", "ab", "bc", "A", "B" and "AB", are statistic
systems.
differences and similarities between agricultural systems.

3.2. Growth of Planted Species

Comparison of models for Caaguazú indicated that the species, agronomic system
and plantation type influenced the growth rate of individuals. In Itapúa, however, on
 Site Model (Intercept) AICc Delta Weight R2m R2c
Caaguazú 40 6,978,656 298.5042 0.000000 946,708.8 0.8671280 0.8733760
Itapúa 2 0.2708572 638.4951 0.000000 888,152.8 0.2894882 0.2924227
Abbreviations are as follows: AICc, Akaike information criterion corrected for a ΔAICc ≤ 2; R2c:
Forests 2022, 13, 2045 8 of 15
conditional R2 indicating the variability explained by the fixed and random effects; R2m, marginal
R2 that considers only the variability explained by the fixed effects.

−1 of native species planted in (a) Caaguazú and (b) Itapúa.

Figure3.3.Relative
Figure Relativegrowth
growthrate
rate(m
(mday
day−1)) of native species planted in (a) Caaguazú and (b) Itapúa.
(c)
(c)Comparison
Comparison of ofrelative
relativegrowth
growthrates
ratesfor
fordifferent
differentagronomic
agronomicsystems
systemsandandplantation
plantation types
types in
in
Caaguazú. The letters “a”, “b”, “c”, “ab”, “abc” and “bc”, are statistical differences and similarities
Caaguazú. The letters "a", "b", "c", "ab", "abc" and “bc”, are statistical differences and similarities be-
tween species
be-tween and
species be-tween
and be-tweenagricultural systems
agricultural systems.

3.3.
3.3.Natural
NaturalRegeneration
Regeneration
Comparison
Comparisonof ofmodels
modelsindicated
indicatedaasignificant
significanteffect
effectof
ofspecies
speciesand
andagronomic
agronomicsystem
system
on the natural regeneration of planted species at both locations (Table 4).
on the natural regeneration of planted species at both locations (Table 4).

Table 4. Plausible models for the regeneration of planted species in the two agroforestry experiments.

Site Model (Intercept) AICc Delta Weight

Caaguazú 22 −193,025,850 159.8007 0.000000 676,183.7
24 −200,038,011 161.6283 1.827547 271,155.1
Itapúa 4 −18.560 130.8007 0.000000 676,183.7
Abbreviations are as follows: AICc, Akaike information criterion corrected for ∆AICc ≤ 2.

Of the six planted species, we observed only non-planted, naturally regenerated in-
dividuals of C. trichotoma, H. albus, and P. dubium (Figure 4 and Table S4c). In addition,
one individual of a non-planted species (Cecropia pachystachya Trécul.) was identified in
Caaguazú. At that site, the number of naturally regenerated H. albus individuals was
higher in the conventional system (3.00 ± 3.43 individuals/plot) than in the agroecological
 Abbreviations are as follows: AICc, Akaike information criterion corrected for ΔAICc ≤ 2.

Of the six planted species, we observed only non-planted, naturally regenerated in-
dividuals of C. trichotoma, H. albus, and P. dubium (Figure 4 and Table S4c). In addition,
one individual of a non-planted species (Cecropia pachystachya Trécul.) was identified in
Forests 2022, 13, 2045 9 of 15
Caaguazú. At that site, the number of naturally regenerated H. albus individuals was
higher in the conventional system (3.00 ± 3.43 individuals/plot) than in the agroecological
system (0.11 ± 0.33 individuals/plot; Figure 4b and Table S4c). In Itapúa, the natural re-
system (0.11of±the
generation 0.33 individuals/plot;
three Figure
mentioned species 4b andbetween
differed Table S4c). In Itapúa,
agronomic the natural
systems, being
regeneration of the three mentioned species differed between agronomic systems,
higher in the agroecological system (0.50 ± 0.80 individuals/plot) than in the conventional being
higher in the
(0.17 ± 0.38 agroecological and
individuals/plot) system (0.50 ±(0.10
traditional 0.80±individuals/plot) thansystems
0.31 individuals/plot) in the conven-
(Figure
tional ± individuals/plot) and traditional (0.10 ±
4 and Table S4c). The agronomic system and plantation type did not affect the systems
(0.17 0.38 0.31 individuals/plot) natural
(Figure 4 and Table S4c). The agronomic system and plantation type did not affect the
regeneration of C. fissilis, H. impetiginosus, or C. americana in Itapúa (Table S4c).
natural regeneration of C. fissilis, H. impetiginosus, or C. americana in Itapúa (Table S4c).

Figure 4. Number of naturally regenerated individuals of (a) Cordia trichotoma, (b) Handroanthus albus,
Figure
and (c) 4. Number of
Peltophorum naturally
dubium regenerated
in Caaguazú andindividuals
Itapúa. Theof (a) Cordia
letters trichotoma,
“a”, “b”, (b)“bc”,
“c”, “ab”, Handroanthus
“A” and
albus, and (c) Peltophorum dubium in Caaguazú and Itapúa. The letters "a", "b", "c", "ab", "bc", "A" and
“B”, are statistical differences and similarities between types of plantations.
"B", are statistical differences and similarities between types of plantations.
4. Discussion
The establishment of native trees and natural regeneration in I. paraguariensis crops in
the Atlantic Forest has rarely been investigated in a systematic fashion. This study analyzed
the establishment (survival and growth) and natural regeneration of six species planted in
different agronomic systems and plantation types in the Atlantic Forest region in Paraguay.
In general, survival, growth, and natural regeneration at the two study sites depended on
the planted species (H1). However, the differences among the agronomic systems (H2) and
plantation types depended on the study site (H3).

4.1. Establishment and Natural Regeneration Depend on the Species

Our results indicated that the species systematically affects survival, growth, and
natural regeneration at the two study sites. Survival averaged 65.9% after six years of
monitoring in Caaguazú and after four years in Itapúa; in some cases, it was higher than
that reported for other species of the same genus. In Venezuela, for example, Cordia thaisiana,
Forests 2022, 13, 2045 10 of 15

Cedrela odorata, and Handroanthus rosea showed survival rates of 56%–81% at 18 months after
planting in the subtropics, while two species of Cedrela showed survival rates of 74 and 81%
at 24 months after planting in the humid tropics [30]. Other studies reported survival rates
of 60% for Cordia alliodora after six years of planting [66] and 50% for C. odorata [67]. In an
agroforestry system in Rwanda, the survival rate for Cedrela spp. and C. trichotoma was
60%, and the mean rate across the 14 studied tree species there was 51% [29]. Additionally,
C. trichotoma survival reached 70% in our study, consistent with a previous report that its
survival rate was higher than that of other species [68].
In our study, a crucial determinant of the survival of planted trees was browsing
by cattle from neighboring farms, which affected 94% of the experimental plots. This
highlights that proper management of livestock is essential in agroforestry [29]. For exam-
ple, in Zambia, owners who controlled their livestock achieved survival rates of 68% in
agroforestry systems, compared to only 32% on farms without this control [69]. Therefore,
raising fences to exclude livestock may significantly increase tree survival rates [70]. Even
so, the survival rates in our studies were higher than those reported in previous work.
We attribute the low survival of C. fissilis not only to cattle browsing but also to the
vulnerability of this species to leafcutter ants, whose presence can be observed from the
first year of planting [71,72], to the mahogany shoot borer Hypsipyla grandella (Zeller),
which commonly infests this species [73,74], and/or to diseases, such as canker fungus
(Botryosphaeriaceous fungi) [75]. In agreement with previous work [76], our field obser-
vations indicated greater attacks of leafcutter ants on C. fissilis than on P. dubium and
H. impetiginosus, and no attacks on C. trichotoma or H. albus, which survived longer than
C. fissilis. Agroforestry systems, by promoting greater biodiversity than simple crops, can
promote the presence of natural enemies of leafcutter ants [77].
The relative growth rate in our study, which averaged 0.00176 m/day−1 across all
species, varied substantially from one species to another. The higher growth rate of
C. trichotoma compared to the other species is consistent with previous observations [78],
and in part it may reflect that the tree participates in mutualism with Hymenoptera, as it
was found between Cordia eliodora and Astecas ants [79]. Conversely, the low growth rate
of C. fissilis can be attributed to attacks by Atta sexdens and H. grandella, as reported in
several studies [80,81]. The higher growth rate in the conventional agronomic system in
Caaguazú may be attributable to soil characteristics (Table S5), such as texture, structure,
soil moisture, and fertility [82], which favor moisture retention, which in turn promotes
water consumption and plant growth [83] or forms of eradication of competitive weeds [84].
In our study, only three species showed natural regeneration. The seedlings of the
pioneers C. trichotoma and P. dubium [85,86] came from seeds of adult congeners located
near the planting plots. The P. dubium species grows fast [85] and its serotinous character
leads to high seed germination [87,88]. Unlike these two species, H. albus flowers at an
early age (in year four), allowing the appearance of seedlings in situ, which is important
because it is a threatened species in Paraguay. Unfortunately, C. fissilis, a threatened species
in Appendix II of the report in [89], did not show regeneration in the experimental plots,
as observed in Costa Rica [90]. This is attributable to the long time needed for C. fissilis
to produce seeds [70] and the absence of nearby mother plants that could export seeds to
agricultural plots [91].
Intensive farms generally have very few or no mature trees [92] and in agroforestry
systems, farmers perform annual plantings that make natural regeneration difficult [93,94].
However, in agroecosystems receiving minimal human intervention, such as natural grass-
lands or conservation areas, many tree species can reproduce naturally [95,96].

4.2. Effects of the Agronomic System and Plantation Types on Establishment and
Natural Regeneration
We tested the hypothesis that agronomic systems would affect the establishment and
natural regeneration of the species, and that agroecological systems would facilitate these
outcomes. This hypothesis was partially confirmed, since growth was similar in different
Forests 2022, 13, 2045 11 of 15

agronomic systems, and natural regeneration was greater in agroecological plantations

only in Itapúa. Higher survival in agroecological than conventional systems is consistent
with previous work [93] on tropical ecosystems in Costa Rica. In our study, the higher
survival can be attributed to two factors. First, the initial soil quality was better in the
agroecological than conventional system; pH was close to neutral, the concentration of
exchangeable aluminum was lower, and there was less compaction and greater depth. This
better edaphic quality in agroecological systems has been repeatedly demonstrated [97,98].
Second, in the conventional system, the use of glyphosate on our experimental plots or
contiguous plots may have weakened the ability of tree seedlings to resist environmental
stress and fungal diseases [99], and these effects can occur up to 20 m from the point of
application, since the wind disperses the glyphosate [100]. In contrast, growth was slightly
higher in the conventional than agroecological system in Caaguazú, which may be due to
the use of insecticides to control leafcutter ants in the first system [30,67], and to the greater
organic matter content and better texture of the conventional soil [5] (initial soil analysis in
the experimental plots is shown in Table S5).
We investigated whether the establishment and natural regeneration would be more
significant in islets than in pathsides and agricultural field edges, since these linear elements
are more exposed to sun, livestock, and wind. This hypothesis was partially confirmed,
since the type of plantation affected both survival and growth in Caaguazú, but it did not
affect natural regeneration at either site. These results could be attributed to the following
two factors: first, the scarcity of mother plants in the vicinity of the plots as sources of
propagules [19]; second, the presence of livestock in the experimental plots due to a lack of
local management [29].

5. Conclusions
The results of this study will help to implement agroforestry systems in the subtropics
of Latin America, particularly in the Atlantic Forest ecoregion. Our data on survival,
relative growth, and natural regeneration for various native tree species can help farmers
select the most appropriate agroforestry species for the cultivation of I. paraguariensis.
Here, C. fissilis has shown susceptibility to disease and attack by leafcutter ants, so
we suggest planting this species only after populations of such ants have been reduced
and populations of their natural enemies have increased in agroforestry plots, which
may be promoted by planting other tree species, such as C. americana, because of its high
survival rate, C. trichotoma, because of its rapid growth, stem uniformity, and resistance
to herbivorous insects, and H. albus, because of its early flowering, which accelerates
natural regeneration.
In this work, agronomic systems and plantation types influenced the survival, growth,
and natural regeneration of the six species in different ways. Given this variability, we
recommend carefully considering the local context of the plots of interest, as well as
considering cattle browsing and trampling as factors that can influence early establishment
of seedlings. Ultimately farmers must make the final decision about the use of plots and
the type of plantation in agroforestry systems, and they should consider all the relevant
factors that can affect growth, survival, and regeneration.

Supplementary Materials: The following supporting information can be downloaded at https://

www.mdpi.com/article/10.3390/f13122045/s1: Figure S1. Plot design; Figure S2. Experiment design
in Caaguazú. Arrangement in (a) path side and islet plots and (b) field edge plots; Figure S3.
Experiment design in Itapúa. Arrangement in (a) plots in the types of plantation and (b) plants on the
plot; Table S1. Type of management in each agronomic system at the two study sites; Table S2. Initial
average height measurements (m) of individuals planted in different experimental plots (p); Table S3.
Plausible models for the survival, growth, and regeneration of planted species in the two agroforestry
experiments; Table S4. Descriptive statistics of the survival, growth, and natural regeneration of
planted species at the two study locations, stratified by agronomic system and plantation type and
Table S5. Initial physical and chemical properties of the soil in the experimental plots in Caaguazú
(Year = 2010).
Forests 2022, 13, 2045 12 of 15

Author Contributions: Conceptualization and methodology, A.I.O., J.M.R.B. and L.C.; data collection,
A.I.O.; formal analysis, A.I.O. and L.C.; validation, A.I.O., L.C. and J.M.R.B.; writing—original draft
preparation, A.I.O.; writing—review and editing, L.C. and J.M.R.B.; supervision, J.M.R.B. All authors
have read and agreed to the published version of the manuscript.
Funding: We thank the Carolina Foundation of Spain and the National University of Asunción for a
doctoral scholarship for A.I. and the National Council of Science and Technology (CONACYT) of
Paraguay for support within the framework of the Scientific and Technological Linkage Program
(PVCT19). We are also grateful to FIRE Paraguay for linking the research with the institutional project
“Restoration of Agricultural Spaces”.
Data Availability Statement: Not applicable.
Acknowledgments: We are grateful to the landowners who voluntarily allowed us access to their
properties, without which this study would not have been possible. Finally, we thank Alice Romero
and Anibal León for fieldwork, and Ulises Riveros and Verónica Cruz-Alonso for statistical support.
Conflicts of Interest: The authors declare no conflict of interest.

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