Forest Ecology and Management 474 (2020) 118389

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Forest Ecology and Management

journal homepage: www.elsevier.com/locate/foreco

Restoration plantings of non-pioneer tree species in open fields, young T

secondary forests, and rubber plantations in Bahia, Brazil
⁎
Daniel Piottoa, , Kevin Flesherb, Andrei Caíque Pires Nunesa, Samir Rolima, Mark Ashtonc,
Florencia Montagninic
a
Centro de Formação em Ciências Agroflorestais, Universidade Federal do Sul da Bahia, BR 415, km 39, Ferradas, Itabuna, BA 45613-204, Brazil
b
Reserva Ecológica Michelin, Km 05 Estrada Ituberá/Camamu, Igrapiúna, Bahia 45443-000, Brazil
c
Yale University, School of Forestry and Environmental Studies, 360 Prospect St., New Haven, CT 06511, USA

A R T I C LE I N FO A B S T R A C T

Keywords: The Atlantic forest of Brazil is a biodiversity hotspot that retains less than 12% of its original area. In this biome,
Forest restoration non-pioneer tree species with limited dispersal are the most impacted by recent habitat loss and fragmentation.
Enrichment planting As attempts to establish non-pioneer tree species in pastures and agricultural fields in the Atlantic forest have
Growth failed, restoration strategies that consider planting these species in other habitats, such as the understory of
Survival
secondary forests and tree plantations may be more successful. To test this, five native non-pioneer tree species
Tropical moist forest
(Sloanea obtusifolia, Garcinia macrophylla, Copaifera lucens, Symphonia globulifera, and Pouteria reticulata) were
planted in complete randomized blocks in April 2009, with four site replications and four treatments (open
fields, open fields with pioneers, young secondary forests, and rubber plantations). Survival, height, and dbh
(diameter at the breast height) were measured every year for six years. We also measured canopy cover and soil
physical and chemical parameters. Six years after planting, we found similar survival of non-pioneer tree species
in open fields, young secondary forests and within rubber plantations. However, height and dbh growth were, in
general, significantly higher in open fields. Planting pioneer species in mixture with non-pioneers did not im-
prove the growth of non-pioneers. We also found differences among species, with Copaifera lucens showing
higher survival and growth than the other species. Even though enriched young secondary forests and rubber
plantations could be important contributors to biodiversity conservation, higher growth rates of non-pioneer
species in open fields have the benefit of accelerating the recovery of wildlife activity in restoration plantings.

1. Introduction
Land clearance by humans has reduced forest cover in the Brazilian
Atlantic forest to 12% of its original extent (Ribeiro et al. 2009). Recent
estimations predict that a third of tree species in the biome may go
extinct because of fragmentation and degradation (Canale et al. 2012,
Silva and Tabarelli 2000). Non-pioneer tree species include a wide
array of long-lived canopy tree species that attain dominance of a forest
later in successional development (Swaine and Whitmore, 1988). Non-
pioneer tree species have limited dispersal and as a large group of
species, they are generally, compared to pioneers, the most affected by
the current habitat loss and fragmentation (Tabarelli and Peres 2002,
Metzger 2000, Tilman et al. 1994) and, consequently, conservation
programs have focused their efforts on these species, e.g. the IUCN Red
List. The main strategy to conserve non-pioneer tree species has been
the creation of protected areas that retain the last remnants of old-
growth forests. However, these relict forests may not be sufficient to
sustain viable populations of non-pioneer tree species, because the old-
growth remnants in the Atlantic forest are too small and frequently lack
the full complement of mammals and birds that act as specialized dis-
persers (Galetti et al. 2013, Silva and Tabarelli 2000).
In Brazil, an increase in the exigencies of environmental laws has
led to a growth in the demand for restoration projects, some of which
are based on mixed plantations of native tree species. These plantations
are usually established in open and isolated areas where secondary
forest succession is unlikely to happen and have included a high di-
versity of non-pioneer and pioneer native tree species (Rodrigues et al.
2009). The use of mixed tree plantations of native species has been
employed as a restoration strategy in the Atlantic forest since the
1970′s. Several plantation designs were developed over the past
50 years, including the random distribution of native species plantings
in open fields (Nogueira 1977), the distribution of native species

⁎
Corresponding author.
E-mail address: daniel.piotto@ufsb.edu.br (D. Piotto).

https://doi.org/10.1016/j.foreco.2020.118389
Received 3 April 2020; Received in revised form 28 June 2020; Accepted 1 July 2020
0378-1127/ © 2020 Elsevier B.V. All rights reserved.
D. Piotto, et al.
plantings in open fields based on the composition of adjacent forests
(Joly et al. 2000), and the most commonly adopted strategy of com-
bining native pioneer and non-pioneer species together in open field
plantings (Kageyama and Castro 1989). This last design assumes that
the shade of pioneer species provides adequate conditions for non-
pioneer species to grow. However, studies have reported extremely low
survival rates of non-pioneer species in these plantations. Souza and
Batista (2004) reported that out of 42 tree species planted only four
pioneer species shared overstory dominance (Cecropia pachystachya,
Croton floribundus, Genipa americana, and Peltophorum dubium) in a
10 year-old plantation. In another area reforested with 39 species, the
same authors found that only two pioneer species (C. floribundus and C.
pachystachya) comprised more than 50% of the total tree density after
9.4 years. Moreover, Brancalion et al. (2018) reported that in addition
to the low survival of non-pioneer species, species with large-sized
seeds (diameter > 12 mm) have been rarely used in Atlantic forest re-
storation projects due to problems associated with their collection,
storage and germination. However, if conservation and restoration ef-
forts are to advance, finding ways to incorporate non-pioneer species
that would be considered relatively rare and dependent upon large
mammals or birds for dispersal needs to be considered.
The poor performance of non-pioneer species when mixed with
pioneers in open areas reinforces the idea that restoration techniques
must be based on a thorough understanding of the species ability to
establish and grow under different environmental conditions (Sayer
et al. 2004). As some attempts to establish non-pioneer tree species in
open full sun areas in the Atlantic forest have failed (Brancalion et al.
2018, Souza and Batista 2004), restoration projects need to consider
other strategies in order to increase the probability of successfully re-
storing populations of these species. There have been several successful
experiences of enrichment planting of non-pioneer species in the un-
derstory of natural forests in the tropics (Atondo-Bueno et al. 2018,
Keefe et al. 2009, Piotto 2007, Montagnini et al. 2006, 1997, Schulze
et al. 1994, Ramos and del Amo 1992). However, few studies have used
the understory of tree plantations to grow non-pioneer tree species
(Rappaport and Montagnini 2014, Ashton et al. 1997). Ashton et al.
(1997) demonstrated that pine plantations can facilitate the establish-
ment of non-pioneer tree species in the mixed dipterocarp forests of
south-east Asia, while Rappaport and Montagnini (2014) showed that
rubber plantations were suitable for enrichment planting of non-pio-
neer trees. Therefore, similar to natural forests, tree plantations may
ameliorate soil and microclimatic conditions, which can favor the es-
tablishment of non-pioneer tree species (Kaewkrom et al. 2005, Cusack
and Montagnini 2004, Keenan et al. 1997, Parrotta 1992).
In this study, we compare the performance of non-pioneer tree
species growing in open areas and within the understory of young
secondary forests and rubber plantations for six years. We also examine
whether mixing pioneer tree species with non-pioneer tree species in
open areas improves the survival and growth of the latter. We hy-
pothesized that after six years: (i) non-pioneer tree species growth and
survival are better beneath partial shade (young secondary forests and
rubber plantations) than in open areas, because microclimatic condi-
tions of the understory will promote the establishment of the more
shade-tolerant non-pioneer tree species; and (ii) in open areas, non-
pioneer tree species growth and survival are better in mixed stands of
pioneer and non-pioneer tree species than in stands of only non-pioneer
tree species, because pioneer tree species can potentially provide partial
shade to non-pioneer species while simultaneously shading out sun-
loving grasses, thereby diminishing competition for soil resources.
2. Materials and methods
2.1. Site description
The Reserva Ecológica Michelin (REM) is located in southern Bahia,
Brazil, in the municipalities of Ituberá and Igrapiúna at 13°50′ south
2
Forest Ecology and Management 474 (2020) 118389
and 39°10′ west. The reserve encompasses an area of 3400 ha of which
1500 ha are a mix of disturbed mature and secondary forests with the
remainder consisting of abandoned rubber plantations and secondary
forests on hilltops and along riparian corridors. In order to increase the
value of the reserve for native species, the reserve management strategy
is to enrich the abandoned rubber plantations with native non-pioneer
species, eventually replacing the rubber plantations with natural forest.
The reserve occupies several hills reaching 95–380 m above sea level
with slopes of more than 30%. The soils are low fertility typic hap-
lorthox soils (Santana et al. 2002). The REM has an average monthly
temperature of 25 °C, receives 1300–2600 mm of precipitation/year
with rainfall throughout the year. The natural vegetation is classified as
tropical moist forest, a four strata vegetation with emergent trees taller
than 35 m (Veloso et al. 1991). Despite having similar forest structure
and sharing some of its flora and fauna with Amazonian forests, the
Bahian coastal forests are considered to be a distinct forest type because
of its high levels of endemism (Mori et al. 1981). An estimated of at
least 547 tree species are thought to be endemic to the Bahian coastal
forests (Ostroski et al. 2018). On a local level, research on the flora of
two reserves in southern Bahia showed that 28.1 and 26.5 percent of
the tree species, respectively, are endemic to the region (Thomas et al.
1998).
2.2. Experimental design
Five native non-pioneer tree species were planted in full sun and
partial shade treatments. Species choice was based on rarity, dispersal
constraints, and availability of seedlings in the region. The species
were: Sloanea obtusifolia (Moric). K. Shum.,‘gindiba’ (SO),
Elaeocarpaceae; Garcinia macrophylla Mart.,‘bacupari’ (GM),
Clusiaceae; Copaifera lucens Dwyer, ‘óleo-copaíba’ (CL), Fabaceae;
Symphonia globulifera L., ‘landirana’ (SG), Clusiaceae; Pouteria reticulata
(Engl.) Eyma, ‘bapeba’ (PR), Sapotaceae. All are slow-growing canopy
species (maximum tree height ranging from 25 to 35 m), with relatively
dense wood (0.6–0.8 g/cm3), medium- to large-sized seeds (dia-
meter > 6 mm), and dependent upon large mammals or birds for dis-
persal (Piotto et al. 2009, Jesus and Rolim 2005, Tabarelli and Peres
2002). Their reintroduction into young secondary forest, old planta-
tions, or as a component of a reforestation planting on open fields can
be an important component of encouraging some of the larger mam-
mals and birds back into the landscape from nearby forests once they
are reproductive, and in restoring a compliment of species of important
conservation value that otherwise would not be present in young forests
or reforestation efforts.
In April 2009, these five native non-pioneer tree species were
planted in two full sun treatments and two partial shade treatments.
Plantings for each treatment were arranged in plots that comprised
complete randomized blocks, with four replications each (Fig. S1).
Treatments were designed to test four different strategies to grow non-
pioneer tree species:
• T1 (full sun, only non-pioneers): Seedlings of the five non-pioneer
tree species were planted in open fields using a spacing of 7 × 3 m.
• T2 (full sun, pioneers and non-pioneers): Seedlings of two native
fast-growing pioneer tree species (Tapirira guianensis Engl., ‘pau-
pombo’, Anacardiaceae and Tachigali densiflora Benth.,‘passuaré’,
Fabaceae) which are commonly found in early successional forests
of the region (Piotto et al. 2009), with initial spacing of 7 × 3 m
were planted in open fields. Simultaneously, seedlings of the five
non-pioneer tree species were planted in between using a spacing of
7 × 3 m.
• T3 (partial shade, secondary forest): One-meter wide lines were
cleared in young secondary forests (10–25 yr old) and seedlings of
the five non-pioneer tree species were planted using a spacing of
7 × 3 m (see Piotto et al. 2009 for details about secondary forest
structure and composition in the region).
D. Piotto, et al.
• T4 (partial shade, rubber plantation): Seedlings of the five non-
pioneer tree species were planted using a spacing of 7 × 3 m in
between rubber tree rows in rubber plantations ranging from 15 to
25 year-old. These rubber plantations were established using a
spacing of 7 × 3 m and had an average basal area of 17.6 m2/ha and
average canopy height of 14.2 m when the experiment was estab-
lished.
To establish these treatments in the field, four sites (blocks) were
selected within the REM and for each site all four combinations
(treatments) of open field, open field with pioneers, second growth and
old rubber plantation were represented. For each site (block) a treat-
ment was represented by single plot with dimensions of 35 × 45 m. In
each plot, 75 seedlings of the five non-pioneer tree species (15 seedlings
of each species) were planted. Guard rows of 7 m were used around the
plots to account for edge effects. Hence, the experimental design
comprised four sites (blocks), each site comprising four treatments,
with each treatment represented by a single plot within which 15
seedlings each of five non-pioneer species were planted. In each plot, a
systematic design was used to maximize species interactions, where
individuals from the five species were alternated by row and each row
had all five species (Fig. S1).
2.3. Soil sampling
Soils were sampled to gain a better understanding of the different
environmental characteristics of the site where the experiments were
conducted, to serve for reference for interpreting results, and to enable
comparisons with other experiences in different settings. However, we
did not intend to examine changes in soil properties as they could be
influenced by the experimental settings, for this reason soil sampling
was performed only once, at the beginning of the research. Before
planting, composite soil samples of 3 sub-samples were taken for each
plot at 14-meter intervals, including the edges and center of the plots.
Soil sub-samples were collected from 0 to 20 cm depth using a hammer
and a 20 cm stainless steel tube and pooled together in labeled plastic
bags. The soil samples were analyzed for physical (CS = Coarse sand;
FS = Fine sand; SI = Silt; CL = Total clay) and chemical properties,
including pH (water), Mehlich-1 extractable phosphorous (P) and po-
tassium (K), exchangeable Calcium (Ca) and Magnesium (Mg) using an
extracting solution and analyzed by atomic absorption, exchangeable
Aluminum (Al) extracted with KCl, total nitrogen (N) by the Kjeldahl
method, and total carbon (C) and organic matter (OM) by the Tiurin
method. All soil analyses were performed at the Centro de Pesquisas do
Cacao (CEPEC/CEPLAC) soil laboratory. One-way analyses of variance
were used to compare soils chemical and physical parameters among
four replications and four treatments, followed by a Scott-Knott test
with significance level set at p < 0.05 (Scott and Knott 1974).
2.4. Light environments
In 2009 (right after planting), 2011, and 2013, percent canopy
cover was measured in each treatment plot using a spherical densi-
ometer consisting of a cross-shaped grid scratched on the convex sur-
face of a mirror (Lemmon 1956). The densiometer was held leveled at
waist height and estimates of percent canopy cover were taken at the
center of each plot facing each cardinal direction (N, S, E and W). Es-
timates were then averaged for each sample point. The averages of
canopy cover (%) were calculated for each treatment and year.
2.5. Plantation measurements and statistical analysis
In each plot, height, dbh (diameter at the breast height – 130 cm
from soil surface), and survival were measured for each planted tree
every year for a total of six years. The averages of total height, dbh and
survival were calculated for each plot, species and treatment. In order
3
Forest Ecology and Management 474 (2020) 118389
to compare the effect of treatments and species on height, dbh, and
survival in the last year of measurement, an analysis of variance, con-
sidering the effects of site (block), species, treatments and interaction
between treatments and species was conducted followed by a Scott-
Knott test. For height and dbh, a Box–Cox transformation was used to
correct for non-normality (Box and Cox 1964). For survival, we used
species survival at the plot level for the analysis. All analyses were
performed in the software R, version 3.6.0 (R Core Team 2019).
3. Results
Soil analysis showed no significant differences among sites and
treatments for soil physical properties and for most soil chemical
properties. Only exchangeable Aluminum (Al) was significantly lower
in T1 (full sun non-pioneer planting) and significantly higher in one
replication (Varjão). Mean soil pH was significantly higher in the “Vila
9” block (Table S1). For the first four years after planting percent ca-
nopy cover did not change within each treatment for T1 (full sun, non-
pioneer planting), T3 (partial shade, secondary forest) and T4 (partial
shade, rubber plantation). However, by the fourth year T2 (full sun,
pioneers with non-pioneers) had an increase in canopy cover from 0 to
42.3% (Table 1).
Six years after planting, there were statistically significant differ-
ences for height, dbh and survival among sites (replications), treat-
ments and species (Fig. 1, Table 2). In general, treatments of full sun
showed mean height and mean dbh significantly higher than partial
shade treatments (Fig. 1, Table S2). From four to six years after
planting, T2 (full sun, pioneers with non-pioneers) showed a significant
decrease of mean dbh when compared to T1 (full sun non-pioneer
planting) (Fig. S2). Survival of trees in full sun treatments was similar to
that of in secondary forests (T3) and rubber plantations (T4) (Fig. 1,
Table S2). After six years, Copaifera lucens had the highest mean height
and dbh (Fig. S3); whereas Symphonia globulifera showed the lowest
survival (Fig. 1, Table S2). The interaction between treatments and
species was significant for height, dbh, and survival (Table 2). While
full sun treatments (T1 and T2) showed no difference in survival or
height among species, dbh was higher for non-pioneers planted without
the competition for space with the pioneers for four out of five species
(CL, GM, SG, and SO). For partial shade treatments (T3 and T4), all tree
species exhibited similar survival and mean height (except SG) in sec-
ondary forests and rubber plantations, but three out of five species (CL,
SG, and SO) exhibited higher mean dbh in rubber plantations. (Fig. 1,
Table S2).
4. Discussion
In our study, we found similar survival of non-pioneer tree species
in open fields, young secondary forests and within rubber plantations,
despite our assumption that the partial shade environment of rubber
plantations and secondary forests is more suitable for non-pioneer
species survival. In contrast with our hypothesis, height growth of non-
pioneer species was significantly higher in open fields (T1 and T2) for
three species (CL, PR, and SO) and dbh growth was significantly higher
Table 1
Means of canopy cover (%) and standard deviation for every treatment in 2009
(right after planting), 2011 (2 years after planting), and 2013 (4 years after
planting), in experimental plantings in southern Bahia, Brazil. T1 = full sun,
only non-pioneers, T2 = full sun, pioneers and non-pioneers, T3 = partial
shade, secondary forest, T4 = partial shade, rubber plantation.
Treatment 2009 2011 2013
T1 0 0 0.8 ± 1.5
T2 0 17.8 ± 16 42.3 ± 27.9
T3 68.8 ± 22.4 68.8 ± 19.6 72.5 ± 12.4
T4 77.5 ± 25.8 76.8 ± 23.9 79.3 ± 11.6
D. Piotto, et al. Forest Ecology and Management 474 (2020) 118389

Fig. 1. Box and whisker plots showing the difference across treatments for each species for height (m), diameter at breast height (dbh, cm), and survival in 6-year old
experimental plantings in southern Bahia, Brazil. T1 = full sun, only non-pioneers, T2 = full sun, pioneers and non-pioneers, T3 = partial shade, secondary forest,
T4 = partial shade, rubber plantation. CL = Copaifera lucens, GM = Garcinia macrophylla, PR = Pouteria reticulata, SG = Symphonia globulifera, SO = Sloanea
obtusifolia. Boxes with different colors indicate significant difference (alpha = 0.05) for treatment means.

in T1 (full sun, only non-pioneers) for four out of five species (CL, GM,
SG, and SO). We also found statistically significant differences in soil
properties for only two parameters (pH and Al), but these differences
were found in only one treatment and one block. This suggests that soil
properties did not contribute to explain differences in tree species
performance. Instead, results suggest the soil properties were not het-
erogeneous enough to explain any of the observed trends.
We also found significant differences among species, with Copaifera
lucens having, in general, higher growth and survival than the other
species tested. Differences in growth and survival among the non-pio-
neers may be related to differences in their functional traits. To try and
tease out these differences clearly demands more refined studies that
can identify traits that predict vital rates under specific environmental
conditions among non-pioneers that can then be associated with their
unique growth parameters (Paine et al. 2015). However, for our study,
for the species we selected, the lack of a trade-off between growth and
survival in general among all five species poses an important question
about the most feasible strategy to increase populations of non-pioneer
tree species in deforested landscapes, whether it be by enrichment
plantings beneath shaded canopies or full sun plantings.
Forest restoration projects in open areas aim to restore both fast
growing pioneer species and those of more late-successional stages.
Pioneer species are commonly used to restore ecosystem properties,
since most pioneer species grow quickly and aid in recovering soil
properties, accelerating succession of formerly degraded lands
(Guariguata and Ostertag, 2001). However, in contrast with our hy-
pothesis, our results show that the non-pioneer tree species used in this
study were not positively affected by mixing with pioneer species. In
our study, this was observed for all non-pioneer species when com-
paring open treatments with and without pioneers. Although pioneer
species may facilitate the establishment of non-pioneer species by al-
tering some microclimatic conditions as predicted in successional

Table 2
Summary of variance analysis including the effect sizes (η2) for height (m), diameter at breast height (dbh, cm) and survival in 6-year old experimental plantings in
southern Bahia, Brazil.
Height dbh Survival

Factors Df η2 P-value Df η2 P-value Df η2 P-value

Block 3 0.09 2.00E−16 3 0.11 2.00E−16 3 0.10 2.98E−03

Treatment 3 0.12 2.00E−16 3 0.17 2.00E−16 3 0.03 0.23292
Species 4 0.09 2.00E−16 4 0.08 2.00E−16 4 0.45 8.15E−10
TxS 12 0.03 0.00238 12 0.03 1.32E−03 12 0.08 0.44134
Residuals 751 0.67 – 705 0.62 – 57 0.35 –

*Df: degrees of freedom.

4
D. Piotto, et al.
theory and can quickly attract fauna that facilitates the colonization by
other species (Viani et al. 2015), in our study this did not improve the
performance of non-pioneers, similar to other results reported by
Campoe et al. (2010) and Delagrange et al. (2008). In fact, because
growth rates, as measured using dbh increment, were higher for four
out of the five non-pioneer species when planted without pioneers,
these species may reach maturity and become functionally active for
wildlife earlier when planted in the full open than the other treatments.
Pioneers are usually abundant in open and/or degraded landscapes,
with seeds generally dispersed by wind and generalist small bats and
birds (Jacomassa and Pizo 2010, Medellin and Gaona 1999) that then
can germinate and self-recruit naturally. On the other hand, non-pio-
neer trees, especially those that have large seeds and depend on animal
dispersal for recruitment, generally must be planted to restore their
populations in degraded landscapes. Pioneer species are short-lived,
and thus restored areas that use a high proportion of pioneer species
can revert back to arrested or interrupted stages of succession (Souza
and Batista 2004). This is common in highly fragmented landscapes
such as the Atlantic Forest of Brazil, where the distance between forest
remnants are frequently greater than 1500 m (Ribeiro et al. 2009),
which is greater than the threshold for non-pioneer species dispersal
and establishment suggested for this region (Suganuma et al. 2018,
Rodrigues et al. 2009, Bertoncini and Rodrigues 2008).
In addition, the timber of pioneer species is generally of low value,
and thus does not offer an incentive for farmers to grow them.
Therefore, the use of tree species that belong to more advanced stages
of succession is also desirable to counteract these challenges. Based on
the results of this study, we suggest that in mixed plantations used for
restoring degraded areas, the proportion of short-lived pioneer species,
which is usually 50%, can be diminished. Thus, restoration projects
using mixed plantations could include higher proportions of non-pio-
neer trees in the species mix. Further study on the costs of seed col-
lection and the economics of nursery propagation for non-pioneer
species should be done to identify species that are easy to collect and
cheap to propagate but that exhibit high growth and survival.
One of the most promising techniques for establishing non-pioneer
tree species has been the enrichment planting in degraded/over-
exploited forests, as well as in existing plantations, as shown by ex-
periences carried out in the Neotropics (Atondo-Bueno et al. 2018,
Keefe et al. 2009, Piotto, 2007, Montagnini et al. 2006, 1997, Ramos
and del Amo, 1992) and in SE Asia (Ashton et al. 1997, Schulze et al.
1994). Non-pioneer-species have high photosynthetic plasticity, high
acclimation capacity, and low compensation points (Souza et al. 2010),
and they can grow in low-light conditions (Veneklaas and Poorter
1998). However, in some situations in very dense and tall forests, such
as mature forests of Costa Rica, non-pioneer tree species presented little
capacity to grow under shade and exhibited high mortality rates (Piotto
2007). Even though our results show that growth rates were lower in
partial shade treatments, young secondary forests and rubber planta-
tions can also serve as nurses for non-pioneer tree species in the long
term because of their steady growth rates. The performance of non-
pioneer species was slightly better in rubber plantations than in sec-
ondary forests, probably because of less competition for growing space
and more seasonal light availability in rubber plantations. The decid-
uousness of rubber trees, their regular spacing, and the fact that the
widespread infection of Neotropical rubber plantations with South
American lead blight (Microcyclus uleii) reduces canopy cover all allow
greater amounts of total and seasonal light penetration into the un-
derstory, favoring growth and survival of seedlings. Nevertheless,
growth rates in enrichment plantings may be improved by canopy
clearing in secondary forests or by periodic thinnings of the canopy in
forest plantations. Canopy thinnings and cleaning or liberation release
treatments (sensu Ashton and Kelty 2018) of advance regeneration and
enrichment plantings can be used for biomass, pulpwood, and con-
struction timber depending upon markets and the dimension, wood
quality and species composition of the trees removed (Swinfield et al.
5
Forest Ecology and Management 474 (2020) 118389
2016, Ashton et al. 1998, 1997). Liberation release can be used to favor
the understory plantings by removing considerably older trees of either
plantation or natural forest origin in the canopy (Ashton et al. 1998,
1997). However, cleaning release can be used to remove competition,
often pioneers of the same cohort, immediately above the plantings or
natural regeneration (Swinfield et al. 2016).
Finally, there is a trade-off between landscape configuration, cost,
and habitat type for the most feasible strategy to increasing populations
of non-pioneer tree species in degraded landscapes. Restoration plant-
ings are generally expensive (Kimball et al. 2015, Preece et al. 2012,
Rodrigues et al. 2009) and this high cost necessarily influences re-
storation strategies. Young secondary forests have a potential for re-
storation through natural succession (Rozendaal et al. 2019). However,
when non-pioneer tree species are absent, forest succession becomes
arrested due to the inability of their seeds to reach degraded sites (van
Breugel et al. 2013) or when secondary forests are the only sources of
seeds for the colonization of cleared sites. In this case, enrichment
plantings become a necessary option to increase the populations of non-
pioneer tree species (Atondo-Bueno et al. 2018, Schwartz et al., 2017),
despite their limited growth rates in partial shade. However, conditions
in shade and overstory structure may change after six years to become
more favorable or unfavorable for growth of non-pioneer enrichment
plantings. This needs to be further monitored over time.
5. Conclusions
Knowledge about feasible ways of increasing populations of non-
pioneer tree species is still very scarce. In our study, we found similar
survival of non-pioneer tree species in young secondary forests and
within rubber plantations as compared to open fields, at least for the
first six years after planting. However, in general, height and diameter
growth were significantly higher in seedlings planted in open fields,
suggesting that restoration plantings for non-pioneer species may be
more successful when in open areas with a higher proportion of non-
pioneers in the species mix.
Even though enriched young secondary forests and rubber planta-
tions could be important contributors to biodiversity conservation,
higher growth rates of some non-pioneer species in open fields have the
benefit of accelerating the recovery of wildlife activity in restoration
plantings and potentially implies a much less costly investment in the
long term. Obviously, further monitoring will be necessary over the
next ten-to-fifteen years to assess these results in relation to the even-
tual success of these plantings to grow and survive.
CRediT authorship contribution statement
Daniel Piotto: Conceptualization, Formal analysis, Funding acqui-
sition, Investigation, Methodology, Writing - review & editing. Kevin
Flesher: Funding acquisition, Investigation, Writing - original draft,
Writing - review & editing. Andrei Caíque Pires Nunes: Formal ana-
lysis, Writing - review & editing. Samir Rolim: Writing - review &
editing. Mark Ashton: Conceptualization, Methodology, Supervision,
Writing - review & editing. Florencia Montagnini: Conceptualization,
Methodology, Supervision, Writing - review & editing.
Declaration of Competing Interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influ-
ence the work reported in this paper.
Acknowledgements
We thank André Souza dos Santos and Manuel da Lapa Conceição de
Assunção (Tipó) for their assistance during the field measurements.
D. Piotto, et al.
Financial support was provided by Reserva Ecológica Michelin.
Appendix A. Supplementary material
Supplementary data to this article can be found online at https://
doi.org/10.1016/j.foreco.2020.118389.
References
Ashton, P.M.S., Gamage, S., Gunatilleke, I.A.U.N., Gunatilleke, C.S., 1997. Restoration of
Sri Lankan rain forest: using Caribbean pine as a nurse for establishment late suc-
cessional tree species. J. Appl. Ecol. 34, 915–925.
Ashton, P.M.S., Gamage, S., Gunatilleke, I.A.U.N., Gunatilleke, C.V.S., 1998. Using
Caribbean pine to establish a mixed plantation: testing effects of pine canopy removal
on plantings of rain forest tree species. For. Ecol. Manage. 106 (2–3), 211–222.
Ashton, M., Kelty, M., 2018. The Practice of Silviculture: Applied Forest Ecology. John
Wiley & Sons Ltd, West Sussex.
Atondo-Bueno, E.J., Bonilla-Moheno, M., López-Barrera, F., 2018. Cost-efficiency analysis
of seedling introduction vs. direct seeding of Oreomunnea mexicana for secondary
forest enrichment. For. Ecol. Manage. 409, 399–406.
Bertoncini, A.P., Rodrigues, R.R., 2008. Forest restoration in an indigenous land con-
sidering a forest remnant influence (Avaí, São Paulo State, Brazil). For. Ecol. Manage.
255, 513–521.
Box, G.E.P., Cox, D.R., 1964. An analysis of transformations. J. Roy. Stat. Soc. 26 (2),
211–252.
Brancalion, P.H.S., Bello, C., Chazdon, R.L., Galetti, M., Jordano, P., Lima, R.A.F.,
Medina, A., Pizo Jr., M.A., Reid, L., 2018. Maximizing biodiversity conservation and
carbon stocking in restored tropical forests. Conserv. Lett. 8 (11), e12454.
Campoe, O.C., Stape, J.L., Mendes, J.C.T., 2010. Can intensive management accelerate
the restoration of Brazil’s atlantic forests? For. Ecol. Manage. 259 (9), 1808–1814.
Canale, G.R., Peres, C.A., Guidorizzi, C.E., Gatto, C.A.F., Kierulff, M.C.M., 2012. Pervasive
defaunation of forest remnants in a tropical biodiversity hotspot. PLoS ONE 7 (8),
e41671.
Cusack, D., Montagnini, F., 2004. The role of native species plantations in recovery of
understory woody diversity in degraded pasturelands of Costa Rica. For. Ecol.
Manage. 188, 1–15.
Delagrange, S., Potvin, C., Messier, C., Coll, L., 2008. Linking multiple-level tree traits
with biomass accumulation in native tree species used for reforestation in panama.
Trees 22 (3), 337–349.
Galetti, M., Guevara, R., Côrtes, M.C., Fadini, R., Von Matter, S., Leite, A.B., Labecca, F.,
Ribeiro, T., Carvalho, C.S., Collevatti, R.G., Pires, M.M., Guimarães Jr., P.R.,
Brancalion, P.H., Ribeiro, M.C., Jordano, P., 2013. Functional extinction of birds
drives rapid evolutionary changes in seed size. Science 340 (6136), 1086–1090.
Guariguata, M., Ostertag, R., 2001. Neotropical secondary forest succession: changes in
structural and functional characteristics. For. Ecol. Manage. 148, 185–206.
Jacomassa, F.A.F., Pizo, M.A., 2010. Birds and bats diverge in the qualitative and
quantitative components of seed dispersal of a pioneer tree. Acta Oecol. 36 (5),
493–496.
Jesus, R.M., Rolim, S.G., 2005. Fitossociologia da Mata Atlântica de tabuleiro. Bol.
Técnico SIF 19. Viçosa, Brazil.
Joly, C.A., Spigolon, J.R., Lieberg, S.A., Aidar, M.P.M., Zickel, C.S., Metzger, J.P.W., Lobo,
P.C., Shimabukuro, M.T., Marques, M.C.M., Salino, A., 2000. Projeto Jacaré-Pepira -
os resultados do desenvolvimento de um modelo de recomposição da vegetação do
ecótono ciliar com base na florística regional. In: Rodrigues, R.R., Leitão-Filho, H.F..
(Org.). Matas ciliares: conservação e recuperação. São Paulo, 2000, v. 01, p. 271–287.
Kaewkrom, P., Gajaseni, J., Jordan, C.F., Gajaseni, N., 2005. Floristic regeneration in five
types of teak plantations in Thailand. For. Ecol. Manage. 210, 351–361.
Kageyama, P.Y., Castro, C.F.A., 1989. Sucessão secundária, estrutura genética e
plantações de espécies arbóreas nativas. IPEF 41 (42), 83–93.
Keefe, K., Schulze, M.D., Pinheiro, C., Zweede, J.C., Zarin, D., 2009. Enrichment planting
as a silvicultural option in the eastern Amazon: Case study of Fazenda Cauaxi. For.
Ecol. Manage. 258 (9), 1950–1959.
Keenan, R., Lamb, D., Woldring, O., Irvine, T., Jensen, R., 1997. Restoration of plant
biodiversity beneath tropical tree plantations in Northern Australia. Forest Ecol.
Manage. 99, 117–131.
Kimball, S., Lulow, M., Sorenson, Q., Balazs, K., Fang, Y.C., Davis, S.J., Connell, O.,
Huxman, T.E., 2015. Cost-effective ecological restoration. Restor. Ecol. 23 (6),
800–810.
Lemmon, P.E., 1956. A spherical densiometer for estimating forest overstory density. For.
Sci. 2, 314–320.
Medellin, R.A., Gaona, O., 1999. Seed dispersal by bats and birds in forest and disturbed
habitats of Chiapas, Mexico. Biotropica 31 (3), 478–485.
Metzger, J.P., 2000. Tree functional group richness and landscape structure in a Brazilian
tropical fragmented landscape. Ecol. Appl. 10, 1147–1161.
Montagnini, F., Eibl, B., Grace, L., Maiocco, D., Nozzi, D., 1997. Enrichment planting in
overexploited tropical forests of the Paranaense region of Misiones, Argentina. For.
Ecol. Manage. 99, 237–246.
Montagnini, F., Eibl, B., Fernández, R., 2006. Rehabilitation of degraded lands in
Misiones, Argentina. Bois et Forets des Tropiques 288, 51–65.
Mori, S.A., Boom, B.M., Prance, G.T., 1981. Distribution patterns and conservation of
Forest Ecology and Management 474 (2020) 118389
eastern Brazilian coastal forest tree species. Brittonia 33, 233–245.
Nogueira, J.O.B., 1977. Reflorestamento heterogêneo com essências indígenas. Boletim
técnico. Instituto Florestal, São Paulo 24, 1–14.
Ostroski, P., Saiter, F.Z., Amorim, A.M., Fiaschi, P., 2018. Endemic angiosperms in Bahia
Coastal Forests, Brazil: an update using a newly delimited area. Biota Neotropica 18
(4), e20180544.
Paine, C.E., et al., 2015. Globally, functional traits are weak predictors of juvenile tree
growth, and we do not know why. J. Ecol. 103 (4), 978–989.
Parrotta, J.A., 1992. The role of plantation forests in rehabilitating degraded tropical
ecosystems. Agric. Ecosyst. Environ. 41 (2), 115–133.
Piotto, D., 2007. Growth of native tree plantations in open pasture, young secondary
forest, and mature forest in humid tropical Costa Rica. J. Trop. For. Sci. 19, 86–96.
Piotto, D., Montagnini, F., Thomas, W., Ashton, M., Oliver, C., 2009. Forest recovery after
swidden cultivation across a 40-year chronosequence in the Atlantic forest of
southern Bahia, Brazil. Plant Ecol. 205, 261–272.
Preece, N.D., van Oosterzee, P., Lawes, M.J., 2012. Planting methods matter for cost-
effective rainforest restoration. Ecol. Manage. Restor. 14 (1), 63–66.
R Core Team, 2019. R: A language and environment for statistical computing. R
Foundation for Statistical Computing, Vienna, Austria. Available at: URL https://
www.R-project.org/.
Ramos, J.M., del Amo, S., 1992. Enrichment planting in a tropical secondary forest in
Veracruz, Mexico. For. Ecol. Manage. 54, 289–304.
Rappaport, D., Montagnini, F., 2014. Tree species growth under a rubber (Hevea brasi-
liensis) plantation: Native restoration via enrichment planting in southern Bahia,
Brazil. New Forests 45 (5), 715–732.
Ribeiro, M.C., Metzer, J.P., Martensen, A.C., Ponzoni, F.J., Hirota, M.M., 2009. The
Brazilian Atlantic Forest: How much is left, and how is the remaining forest dis-
tributed? Implications for conservation. Biol. Conserv. 142 (6), 1141–1153.
Rodrigues, R.R., Lima, R.A.F., Gandolfi, S., Nave, A.G., 2009. On the restoration of high
diversity forests: 30 years of experience in the Brazilian Atlantic Forest. Biol. Conserv.
142 (6), 1242–1251.
Rozendaal, D.M.A., Bongers, F., et al., 2019. Biodiversity recovery of Neotropical sec-
ondary forests. Science. Advances 5 (3), eaau3114.
Santana, S.O., Santos, R.D., Lopes, I.A., Jesus, R.M., Araujo, Q.R., Mendonça, J.R.,
Calderano, S.B., Faria Filho, A.F. 2002. Solos da região sudeste da Bahia: atualização
da legenda de acordo com o sistema brasileiro de classificação de solos. CEPLAC/
EMBRAPA, Rio de Janeiro.
Sayer, J., Chokkalingam, U., Poulsen, J., 2004. The restoration of forest biodiversity and
ecological values. For. Ecol. Manage. 201, 3–11.
Schulze, P.C., Leighton, M., Peart, D.R., 1994. Enrichment planting in selectively logged
rain forest: a combined ecological and economic analysis. Ecol. Appl. 4, 581–592.
Schwartz, G., Pereira, P.C.G., Siviero, M.A., Pereira, J.F., Ruschel, A.R., Yared, J.A.G.,
2017. Enrichment planting in logging gaps with Schizolobium parahyba var. amazo-
nicum (Huber ex Ducke) Barneby: A financially profitable alternative for degraded
tropical forests in the Amazon. For. Ecol. Manage. 390, 166–172.
Scott, A.J., Knott, M., 1974. Cluster analysis method for grouping means in the analysis of
variance. Biometrics 30, 507–512.
Silva, J.M.C., Tabarelli, M., 2000. Tree species impoverishment and the future flora of the
Atlantic forest of northeast Brazil. Nature 404, 72–74.
Souza, F.M., Batista, J.L.F., 2004. Restoration of seasonal semideciduous forests in Brazil:
influence of age and restoration design on forest structure. For. Ecol. Manage. 191,
185–200.
Souza, G.M., Sato, A.M., Ribeiro, R.V., Prado, C.H.B.A., 2010. Photosynthetic responses of
four tropical tree species grown under gap and understorey conditions in a semi-
deciduous forest. Brazilian J. Botany 33 (4), 529–538.
Suganuma, M.S., Torezan, J.M.D., Durigan, G., 2018. Environment and Landscape Rather
than Planting Design Are the Drivers of Success in Long-Term Restoration of Riparian
Atlantic Forest. Appl. Veg. Sci. 21 (1), 76–84.
Swaine, M.D., Whitmore, T.C., 1988. On the definition of ecological species groups in
tropical rain forests. Vegetatio 75 (1–2), 81–86.
Swinfield, T., Afriandi, R., Antoni, F., Harrison, R.D., 2016. Accelerating tropical forest
restoration through the selective removal of pioneer species. For. Ecol. Manage. 381,
209–216.
Tabarelli, M., Peres, C.A., 2002. Abiotic and vertebrate seed dispersal in the Brazilian
Atlantic forest: implications for forest regeneration. Biol. Conserv. 106, 165–176.
Thomas, W.W., Carvalho, A.M., Amorim, A.M., Garrison, J., Arbelaez, A.L., 1998. Plant
endemism in two forests in southern Bahia, Brazil. Biodiversity Conserv. 7, 311–322.
Tilman, D., May, R.M., Lehman, C.L., Nowak, M.A., 1994. Habitat destruction and the
extinction debt. Nature 371, 65–66.
van Breugel, M., Hall, J.S., Craven, D., Bailon, M., Hernandez, A., Abbene, M., van
Breugel, P., 2013. Succession of ephemeral secondary forests and their limited role
for the conservation of floristic diversity in a human-modified tropical landscape.
PLoS ONE 8 (12), e82433.
Veloso, H.P., Rangel-Filho, A.R.L., Lima J.C.A. 1991. Classificação da vegetação brasileira
adaptada a um sistema universal. IBGE, Rio de Janeiro.
Veneklaas, E.J., Poorter, L. 1998. Growth and carbon partitioning of tropical tree seed-
lings in contrasting light environments. Inherent variation in plant growth.
Physiological mechanisms and ecological consequences. Backhuys Publishers,
Leiden, pp 337–361.
Viani, R.A.G., Vidas, N.B., Pardi, M.M., Castro, D.C.V., Gusson, E., Brancalion, P.H.S.,
2015. Animal-dispersed pioneer trees enhance the early regeneration in atlantic
forest restoration plantations. Natureza & Conservação 13 (1), 41–46.