Forest Ecology and Management 438 (2019) 224–232

Contents lists available at ScienceDirect

Forest Ecology and Management

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

Evaluating the success of direct seeding for tropical forest restoration over T
ten years
Marina Guimarães Freitasa,b, Silvia Barbosa Rodriguesc,b, Eduardo Malta Campos-Filhod,
Guilherme Henrique Pompiano do Carmod, Junior Micolino da Veigad,
Rodrigo Gravina Prates Junqueirad, Daniel Luis Mascia Vieirab,
⁎

a
Graduate Degree Program in Forest Science, Universidade de Brasília, Brazil
b
Embrapa Recursos Genéticos e Biotecnologia, Parque Estação Biológica, PqEB, Av. W5 Norte (final), Brasília, DF 70770-917, Brazil
c
Graduate Degree Program in Ecology, Universidade de Brasília, Brazil
d
Instituto Socioambiental, SCLN 210, Bloco C, sala 112, Brasília, DF 70862-530, Brazil

ARTICLE INFO ABSTRACT

Keywords: Direct seeding is considered a feasible alternative for large-scale forest restoration, but little is known about the
Succession successional trajectory of tropical forests restored through direct seeding. To validate this method, we must
Ecological restoration understand how it changes forest structure and species richness and shapes the community trajectory as com-
Chronosequence pared to the standard methods of natural regeneration and seedling planting. We evaluated restoration sites up
Tree density
to 10 years old in the Xingu river basin in Mato Grosso, Brazil. Our objectives were to: (i) describe changes in
Seedlings
Biomass
vegetation structure and richness in restored forests within the first decade; (ii) compare the outcome of re-
storation by direct seeding (broadcast seeding, sowing in rows, or placing seeds in holes) to seedling planting and
natural regeneration; (iii) evaluate the influence of environmental variables (annual precipitation, soil phos-
phorus content, sand percentage, and soil base saturation) and the direct seeding technique on forest structure.
We assessed species richness, density of individuals per size class, basal area, canopy height, aboveground
biomass, and canopy cover. We sampled 72 direct-seeded sites between 1 and 10 years old, three seedling
planting sites and six natural regeneration sites aged 7 to 9 years old. Community structure attributes changed
over time, with the exception of the density of regenerating individuals. After four years, direct-seeded sites had
formed a multi-layered canopy and were starting to be colonized by non-planted species. In general, direct-
seeded sites had high aboveground biomass, but there was high variability among sites, especially after age six
years. Sites with higher phosphorus content had more tree density, basal area, and biomass compared to the
others. Broadcast seeding sites had higher seedling and sapling densities than sites that received other re-
storation methods. In conclusion, direct seeding was a successful method for the initial phase of forest re-
storation, promoting a structure that was more similar to resilient natural regeneration sites than to non-resilient
natural regeneration sites and seedling planting sites.

1. Introduction
Large-scale agriculture and cattle ranching are the main causes of
Amazon deforestation (Macedo et al., 2013; Neill et al., 2013). The
most affected region is the agricultural frontier along the eastern and
southern boundaries of the Amazon, known as “Arc of Deforestation”
(Costa and Pires, 2010). Since 2005, different mechanisms have been
implemented to reduce deforestation and increase forest restoration. In
the Brazilian Amazon, the restoration of more than 8 Mha is mandated
by law (Soares-Filho et al., 2014). Ecological, social, and cost-effective
restoration methods are needed to accomplish this massive obligation
(Campos-Filho et al., 2013; Holl and Aide, 2011; Nunes et al., 2017).
Highly modified, degraded areas with a long history of use may take a
long time to regenerate naturally (Bertacchi et al., 2016; Chazdon and
Guariguata, 2016; Gilman et al., 2016) or may not recover into a sec-
ondary forest (Brancalion et al., 2016). Thus, an active restoration

Corresponding author.
⁎

E-mail addresses: maguimaraesfreitas@gmail.com (M.G. Freitas), silviabrodri@gmail.com (S.B. Rodrigues),

eduardomalta@socioambiental.org (E.M. Campos-Filho), guilhermepompiano@socioambiental.org (G.H.P. do Carmo), junior@socioambiental.org (J.M. da Veiga),
rodrigojunqueira@socioambiental.org (R.G.P. Junqueira), daniel.vieira@embrapa.br (D.L.M. Vieira).

https://doi.org/10.1016/j.foreco.2019.02.024
Received 26 November 2018; Received in revised form 15 February 2019; Accepted 17 February 2019
0378-1127/ © 2019 Elsevier B.V. All rights reserved.
M.G. Freitas, et al.
approach is needed to accelerate and increase the predictability of the
restoration success (Brancalion et al., 2016).
The selection of a restoration method should consider both the so-
cial and environmental characteristics at the local level and the costs
involved (Holl and Aide, 2011). Of the active restoration methods,
seedling planting and direct seeding are the most frequently used
(Brancalion et al., 2016; Grossnickle and Ivetić, 2017; Palma and
Laurance, 2015). Seedling planting can be an effective method to
quickly establish a canopy cover, but it is expensive (Campos-Filho
et al., 2013; Palma and Laurance, 2015); it requires local nurseries,
seedling transportation, and labor for planting (Rodrigues et al., 2009).
Direct seeding is an increasingly used alternative for large-scale re-
storation (Campos-Filho et al., 2013; Grossnickle and Ivetić, 2017).
Seeds are sown through broadcasting, in rows or in holes (Sampaio
et al., 2015) and seedlings establish at high densities (Campos-Filho
et al., 2013; Schneemann and McElhinny, 2012). The costs of labor and
transportation are lower, and direct seeding does not require specific
machinery and nurseries (Balandier et al., 2009; Campos-Filho et al.,
2013; Palma and Laurance, 2015); so costs are only 36% (US$
1845 ha−1) of seedling planting (US$ 5106 ha−1) (Campos-Filho et al.,
2013; Durigan et al., 2013). In the Amazon, the main factors de-
termining the selection of a restoration method are the lack of nurseries
and the need to travel long distances on precarious roads, along with a
relatively high availability of seeds.
Direct seeding has been as an alternative to active restoration of
tropical forests around the globe (Palma and Laurance, 2015). It was
used to restore 5000 ha in the Xingu River basin, and it will be used in
future large-scale restoration projects in the Amazon (Moura, 2018).
Nevertheless, the development of vegetation in this restoration ap-
proach have not been assessed in the region. To validate and adapt this
method, it is essential to know how a forest restored through direct
seeding develops and how it differs from forests restored using other
methods, weighing its costs and benefits (Shoo et al., 2016). Each re-
storation method leaves a signature in the restored forest, particularly
in terms of structure and species and functional composition (Parrotta
and Knowles, 2001, Zahawi et al., 2013, Shoo et al., 2016). In early
secondary forests the structure changes rapidly during the first 10 years
(Lebrija-trejos et al., 2010; Mesquita et al., 2015).
The successional dynamics of tropical forests are quantified by ve-
getation attributes, such as stem density, basal area, species richness
(Norden et al., 2015), and, aboveground biomass, which is important to
assess forest resilience and carbon sequestration (Johnson et al., 2016;
Poorter et al., 2016; Rozendaal et al., 2017). The success of forest re-
storation can be evaluated through ecological indicators, especially
structural attributes, such as canopy cover, seedling density, and
seedling richness (Chaves et al., 2015). These parameters are meant to
indicate that an area at the beginning of restoration process with a
closed canopy cover and high seedling density and richness will follow
the successional trajectory, with no further intervention needed
(Chaves et al., 2015).
Forest growth rate and aboveground biomass accumulation of tro-
pical secondary forests vary with precipitation, soil fertility, and land
use intensity (Chazdon, 2012; Moran et al., 2000; Poorter et al., 2016).
Higher annual precipitation and shorter dry seasons extend the growing
season, increasing the accumulation of aboveground biomass (Johnson
et al., 2016; Poorter et al., 2016; Rozendaal et al., 2017). Higher soil
fertility also increases growth rate and accelerates the rate of above-
ground biomass accumulation in the forest (Melo and Durigan, 2006;
Moran et al., 2000; Toledo et al., 2011). Thus, the success of a re-
storation method is influenced by local factors, such as climate and soil
characteristics.
The Y Ikatu Xingu restoration initiative is an important experiment
in tropical forest restoration due to its scale and level of social en-
gagement (Campos-Filho et al., 2013; Durigan et al., 2013). The method
chosen to restore riparian permanent protection areas in the Xingu
basin river, within the Amazon deforestation arc, that had minimal
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Forest Ecology and Management 438 (2019) 224–232
potential for natural regeneration was direct seeding (Campos-Filho
et al., 2013). In this study, we sampled 72 of the direct-seeded sites,
three seedling planting sites and six natural regeneration sites of
10 years or less. Our objectives were to (i) understand changes in forest
structure over 10 years in the direct seeded sites; (ii) evaluate the in-
fluence of environmental variables on forest structure in the direct
seeded sites. (iii) compare the outcome of the direct seeding method
with seedling planting and natural regeneration. We hypothesized that
seedling density would be relatively high in direct-seeded sites for the
first few years and that the resulting forest would be well stratified into
seedlings, saplings, and trees (Schneemann and Mcelhinny, 2012). This
should be more similar to naturally regenerating resilient sites than to
seedling planting sites, which have a closed homogeneous canopy and a
shady understory (Corbin et al., 2012). We also expected that the ve-
getation structure would be positively influenced by water availability
and soil fertility (Poorter et al., 2016; Moran et al., 2000; Toledo et al.,
2011).
2. Material and methods
2.1. Study area
The study sites were located on the right bank the of Xingu River
watershed, in northeastern Mato Grosso state, Brazil (Fig. 1). Mean
annual precipitation varies from 1491 mm in the south to 2290 mm in
the north (Hijmans et al., 2005). More than 70% of the rainfall is
concentrated between December and March (Ivanauskas et al., 2008).
Mean annual temperature remains above 18 °C throughout the year
(Ivanauskas et al., 2008). The topography is flat with prevalence of red-
yellow latosol (Ivanauskas, 2002). The Xingu River watershed en-
compasses the transition zone between the Amazon (79%) and Cerrado
(20%) biomes, with different vegetation formations. The riparian for-
ests of the Xingu river basin are evergreen seasonal forests (IBGE,
2012). This forest formation has an irregular canopy 10–20 m high,
average basal area of 21 m2 ha−1 and average density of 546 in-
dividuals ha−1 (DBH > 5 cm), with 51–66 species ha−1 (Ivanauskas
et al. 2004). The landscape includes large mechanized soy and corn
farms, pastures, and forest and savanna fragments. Headwater and ri-
parian forests were cleared during the process of occupation of the
region in the 1960s, creating large deforested areas (Teixeira and
Soares-Filho, 2009). Today, the agricultural sector and local govern-
ments, motivated by legal requirements and the need for water con-
servation, are joining forces to restore riparian forests (ISA, 2011). The
Instituto Socioambiental has been working with partners since 2006 to
restore riparian forests in the Xingu basin.
2.2. Restoration methods
The main method used for forest restoration in the studied region
was direct seeding, the focus of our study. The seeds used for direct
seeding were a mixture of native trees and annual and sub-perennial
green manure legumes. Green manure is used to shade the ground for
the first few months to years and improve soil quality, and it is naturally
eliminated by shading (Guerin et al., 2015). Seeding density was 20–40
seeds m−2 of native trees, 6 seeds m−2 of Crotalaria spectabilis Roth, 3
seeds m−2 of Canavalia ensiformis (L.) DC and 1 seed m−2 of Cajanus
cajan (L.) Millsp (Campos-Filho et al., 2013). Half of the tree seeds
(10–20 seeds m−2) were of 15–20 pioneer species that grow quickly
and close the canopy; the other half were of 30–60 late successional
species.
Seeding was carried out by broadcasting with a broadcast spreader
(implement used for spreading pasture grass seeds and lime, common in
cattle farms) attached to a tractor; sowing in rows separated by 50 cm
with end-wheel grain drills (common in mechanized agriculture farms),
in which most of the seeds are put in a fertilizer box mixed with sand; or
by placing seeds directly into 1 × 1 m holes (Campos-Filho et al.,
M.G. Freitas, et al.
Fig. 1. Location of the study area. The black line shows the perimeter of the Xingu River basin. Dots indicate sampled plots of direct seeding (in yellow), seedling
planting (in black), and natural regeneration (in green).
2013). Sowing in rows requires. The type of seeding depends on the
equipment and level of expertise available at the farm; grain farmers
have grain drills, while cattle farmers have broadcast spreaders
(Campos-Filho et al. 2013). For broadcast seeding, the soil is prepared
by repeated plowing months before planting; if necessary, herbicides
are applied in advance to eliminate invasive grasses (Campos-Filho
et al., 2013).
For comparison, we sampled sites with two other common forest
restoration methods, seedling planting and natural regeneration.
Seedling planting (as well as direct seeding sites) was conducted by
restoration technicians in sites with low potential for natural re-
generation, and natural regeneration was allowed to take place in sites
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Forest Ecology and Management 438 (2019) 224–232
presumed to have high potential for natural regeneration. In seedling
planting sites, seedlings were planted at a 3 × 2 m spacing; 50% of the
seedlings belonged to fast-growing species for quick canopy closure,
and 50% corresponded to non-pioneer species, to ensure species di-
versity (Campos-Filho et al., 2013). Natural regeneration sites were
only fenced to prevent the entrance of cattle.
2.3. Sampling plots
Out of 375 sites restored by the Y Ikatu Xingu campaign (https://
www.socioambiental.org/pt-br/tags/campanha-y-ikatu-xingu) we
sampled 72 direct-seeded sites ranging from 1 to 10 years old (48
M.G. Freitas, et al. Forest Ecology and Management 438 (2019) 224–232

broadcasting sites, 12 row sites, 12 hole sites). Restoration sites had 0.5 Table 1
to 50 ha and were 30-m wide, around springs and along small rivers. Vegetation, climate, and soil attributes of direct seeded sites in Mato Grosso,
We selected sites across the precipitation and seasonality gradient, and Brazil.
included different soil types and age ranges. We sampled three seedling Mean Range
planting sites and six natural regeneration sites, ranging in age from
seven to nine years. In each site we established a 50 × 10 m (500 m2) Predictors
Age (years) 5.54 1–10
plot parallel to the water course. Plots were arranged parallel to the
Annual precipitation (mm years−1) 1687 1519–1957
watercourses at a distance of 10 m from both the outer and the inner Phosphorus content (mg dm−3) 2.19 0.30–10.80
edges of the sites, since the sites were 30-m wide. We measured height Base saturation (%) 23.3 6.2–58.3
(H) and diameter at breast height (DBH) for trees and saplings and Sand (%) 61 36–82
Forest cover (%) 18 0–65
diameter at ground level for seedlings. Trees (DBH ≥ 10 cm) were
measured in 500 m2 plots; saplings (height ≥ 1.30 m and Response variables
DBH < 10 cm) were measured in 100 m2 (50 × 2 m); and seedlings Aboveground biomass (Mg ha−1) 22.7 0–77.9
Basal area (m2 ha−1) 7.71 0.04–21.28
(0.30 m ≤ H < 1.30 m) in 25 m2 (50 × 0.5 m) subplots, respectively. Canopy cover (%) 66.9 0.0–94.0
Stems of the same species at least 5 cm apart were considered different Canopy height (m) 6.0 0.6–12.5
individuals. All species were identified in the field if possible or col- Tree density (ind ha−1) 172 0–640
lected for identification at the herbarium of Embrapa Genetic Resources Sapling density (ind ha−1) 5069 0–16,400
Seedling density (ind ha−1) 4972 0–24,400
and Biotecnology (CEN). We used the list of planted species obtained
Total species richness* 13 1–32
from the Instituto Socioambiental reports to distinguish between Non-planted species richness* 2 0–15
planted and non-planted species.
Aboveground biomass (AGB) was estimated for saplings and trees * Species richness within 500 m2 for trees, 100 m2 for saplings, and 25 m2 for
(≥1.30 m tall) using the allometric equation described in Chave et al. seedlings.
(2014) for the BIOMASS package in R software (Réjou-Méchain et al.,
2017). This equation is based on the largest secondary tropical forest correlation between precipitation seasonality and annual precipitation
tree database and uses wood density for calculations (Chave et al., (r = 0.85) and water deficit (r = 0.68). As a result, only annual pre-
2014). We used species-specific wood densities (g cm−3) obtained from cipitation was selected to represent water availability (Table 1).
Neotropical wood density databases (Chave et al., 2009; Zanne et al., We fitted generalized linear mixed-models (GLMMs) with type of
2009; ICRAF Database). We prioritized wood density values from direct seeding (rows, broadcasting and holes) as a random factor and
samples collected near our study area. If plants could not be identified assessed the effects of environmental variables (soil, climate, and
to species we used the values for genus or family. We used a local re- landscape forest cover) on vegetation structure over a 10-year chron-
ference for the wood density of the abundant species Tachigali vulgaris osequence. We used the type of direct seeding method as a random
(Farias et al., 2016). For unidentified morphospecies and species with factor because frequently there were not cases of a seeding type in
no information available, we used the average wood density of all certain ages and environmental conditions. The nine vegetation attri-
species in the database (Chave et al., 2009; Zanne et al., 2009). In this butes (Table 1) did not differ between the three seeding types (analyzed
study, 77.0% of the tree morphospecies were identified to species, by One-Way ANOVAs, restricted to the 7–10 y old sites; data not
14.0% to genus, and 4.5% to family; 4.5% of the morphospecies were shown). We included five interactions between soil and climate vari-
not identified. To calculate carbon stock, we assumed that 50% of AGB ables. There was no strong correlation (r ≤ 0.4) between the variables
consisted of carbon (Chave et al., 2005). Canopy height was estimated entered into the global models. We tested for residual overdispersion of
from the average of the ten tallest individuals. the global models; when detected, overdispersion was corrected by the
inclusion of an observation-level random effect (Harrison, 2014). Re-
2.4. Environmental variables sidual spatial autocorrelation in the global models was verified using
Moran’s I test and corrected with a correction factor estimated using the
We collected soil samples to a depth of 20 cm at three points along package SAM 4.0 (Rangel et al., 2010). We found spatial autocorrela-
each plot. Samples were homogenized and transported to the laboratory tion in two of the response variables tested (total and non-planted
for chemical and physical analyses. We assessed soil organic carbon, species richness), and therefore the influence of spatial distance was
available P, K, Ca, Mg, Fe, and Al, pH, base saturation, and texture included in subsequent analyses. Variables were checked for normality
(sand, silt, and clay). We selected three climatic variables that indicate and stem density was square-root transformed prior to analyses to meet
water availability: annual precipitation and precipitation seasonality, model assumptions. All predictors included in the models were stan-
both obtained from the WorldClim database (Hijmans et al., 2005), and dardized to account for differences in magnitude between variables
climatic water deficit, acquired from http://chave.ups-tlse.fr/ (Table 2). We identified meaningful predictors based on a model se-
pantropical_allometry. Climatic water deficit is the amount of water lection procedure considering all combinations of the variables and
lost in the dry months (defined as months where evapotranspiration interactions included in the global models and using the Akaike In-
exceeds rain), calculated as the difference between rainfall and eva- formation Criterion corrected for small sample sizes (AICc, Burnham
potranspiration during the dry months. To evaluate the influence of the and Anderson, 2002). To assess model performance, we calculated
surrounding forest cover on vegetation attributes, we quantified the differences in AICc values of candidate models as ΔAIC (difference in
area covered by mature forest within a 500-m radius around each plot. AICc value relative to the best-performing model) and Akaike weight
The land-use cover map was obtained from the MapBiomas initiative (wi), which corresponds to the relative likelihood of a given model
(http://mapbiomas.org). (Burnham and Anderson, 2002). We assumed that models with
ΔAIC < 2 were plausible explanations for the data. The relative im-
2.5. Data analysis portance of each variable was compared through regression coefficients
and unconditional standard errors were generated by model averaging.
We selected soil variables by removing highly correlated physical To graphically illustrate the trajectories of each vegetation attribute
and chemical soil variables (r > 0.8) in a Pearson correlation matrix over time we fitted linear and logarithmic regressions and chose the
(Rodgers and Nicewander, 1988). We selected base saturation, phos- highest R2. However, when a vegetation attribute was affected by en-
phorus content, and sand percentage as indicators of soil fertility vironmental variables besides age, we incorporated the effects of the
(Table 1). Precipitation variables were also analyzed, revealing a high most important environmental variable (as indicated by the largest

227
M.G. Freitas, et al. Forest Ecology and Management 438 (2019) 224–232

Table 2 Table 2 (continued)

Model selected to explain the variation in vegetation structure restored through
direct seeding in Mato Grosso, Brazil. Coefficients are shown with 95% con- Model Coefficient 95% CI P
fidence interval (CI) and P-values were extracted from the mean model. Values
Base saturation −0.57 −0.96–−0.19 < 0.001
in bold indicate that the predictor variable was selected (P ≤ 0.05).
Annual precipitation 0.94 0.58–1.29 < 0.001
Model Coefficient 95% CI P Interaction (age and base saturation) 0.08 −0.16–0.64 0.241
Interaction (age and phosphorus) −0.12 −0.73–0.11 0.149
2
Basal area (R = 0.58) Interaction (Annual precipitation and −0.06 −0.58–0.18 0.313
Intercept 2.49 2.08–2.91 < 0.001 base saturation)
Age 0.79 0.56–1.02 < 0.001 Forest cover 0.04 −0.19–0.45 0.402
Phosphorus 0.16 0.01–0.42 0.049 Correction factor −0.32 −3.81–1.54 0.407
Base saturation 0.13 0.01–0.36 0.069 Sand 0.06 −0.56–0.19 0.333
Annual precipitation 0.02 −0.17–0.26 0.707
Interaction (age and phosphorus) 0.07 −0.02–0.38 0.087
Interaction (age and annual precip.) −0.08 −0.54–0.02 0.064 coefficient in the predictive model described above; Table 2). We did
Interaction (age and base saturation) −0.05 −0.34–0.05 0.144
that by fitting two regressions of the vegetation attribute in function of
Aboveground biomass (R2 = 0.60) age, one for a high level and one for a low level of the environmental
Intercept 4.08 3.19–4.97 < 0.001
variable. To determine these levels, we tested five class limits by adding
Age 1.80 1.37–2.22 < 0.001
Phosphorus 0.36 0.03–0.83 0.039
20% steps considering the range of values (e.g. for Soil P ranging from
Base Saturation 0.28 0.02–0.75 0.049 0.3 to 10.8 mg dm-3, we tested five class limits at fixed intervals of
Interaction (age and phosphorus) 0.21 0.01–0.75 0.047 2.1 mg dm-3; thus tested limits were 0.3–2.4 and > 2.4, 0.3–4.5
Forest cover −0.06 −0.57–0.19 0.366 and > 4.5, and so on). The best class limits for each variable were se-
Canopy cover (R2 = 0.38) lected by fitting simple linear and logarithmic models of the vegetation
Intercept 7.50 6.62–8.38 < 0.001 attribute in function of age, one for a high level and one for a low level
Age 1.10 0.50–1.69 < 0.001
of the environmental factor, and assessing the best R2 values. These
Phosphorus 0.25 0.06–0.95 0.091
Interaction (age and annual −0.93 −1.71–−0.32 0.004 different trajectories are plotted for each vegetation attribute vs. age in
precip.) Fig. 2. If there was a second most important variable other than age or
Annual precipitation 0.24 0.26–0.77 0.335 an interaction between two variables, the second variable was also
2
Canopy height (R = 0.53) indicated by different dot sizes in Fig. 2. The high and low level was
Intercept 2.31 2.02–2.60 < 0.001 determined by dividing the values of the variable in two classes of equal
Age 0.47 0.34–0.60 < 0.001 sizes.
Base saturation 0.11 0.01–0.23 0.029
Finally, we compared the vegetation attributes between direct
Sand 0.05 −0.02–0.21 0.129
Interaction (age and base saturation) −0.03 −0.20–0.03 0.148 seeding, natural regeneration, and seedling plantation by means of One-
Annual precipitation 0.02 −0.06–0.16 0.351 Way ANOVAs, restricted to the 7–10 y old sites (the age class with
Tree density (R2 = 0.51) restoration sites using the three restoration methods; Direct
Intercept 10.62 7.27–13.97 < 0.001 seeding = 25 sites; natural regeneration = 6 sites; seedling
Age 5.13 3.58–6.70 < 0.001 planting = 3 sites). Seedling and sapling density were squared-root and
Phosphorus 0.60 −0.61–2.45 0.247 log transformed, respectively, to conform to homoscedasticity and
Interaction (age and phosphorus) 0.90 0.26–3.14 0.020
Annual precipitation 0.34 −0.54–2.28 0.217
normality.
Sand −0.27 −2.36–0.75 0.294
Base saturation 0.41 −0.42–2.32 0.287
Forest cover −0.30 −2.25–0.61 0.285
3. Results
2
Sapling density (R = 0.44)
We recorded 5163 stems in the 72 direct-seeded sites, belonging to
Intercept 58.46 45.87–71.04 < 0.001
Age 12.13 4.91–19.34 < 0.001 155 species, 95 genera, and 42 families. We found 68 species that were
Base saturation 2.29 −2.55–9.34 0.269 absent from the list of planted species. All vegetation attributes, except
Annual precipitation −3.13 −10.00–3.70 0.417 seedling density, increased with site age (Fig. 2). At ten years, sites had
Interaction (age and annual −17.16 −25.69–−8.84 < 0.001
a basal area of 12.5 ± 5.0 m2 ha−1 (mean ± SD), AGB of
precip.)
Forest cover 2.37 −1.05–10.75 0.097
39.5 ± 16.90 Mg ha−1, canopy cover of 98 ± 10%, and canopy
Sand 11.70 5.29–18.33 < 0.001 height of 7.5 ± 2.5 m. Tree, sapling, and seedling densities were
Interaction (age and base saturation) −1.42 −10.72–1.42 0.159 248 ± 210 ind ha−1, 5640 ± 4160 ind ha−1, and 4880 ± 2356 ind
Interaction (annual precipitation and 1.43 −1.36–10.70 0.146 ha−1, respectively. The total number of species reached 15 ± 5, while
base saturation)
the number of non-planted species was 6 ± 4.
Seedling density (R2 = 0.04) The R2 values of the selected models varied between 0.38 and 0.68,
Intercept 62.89 55.46–70.33 < 0.001
and the direction and magnitude of the contribution of each predictor
Age 1.12 −4.30–11.21 0.381
Phosphorus −2.08 −12.53–2.67 0.202 variable varied for each response variable (Table 2). Higher P content
Base saturation −0.76 −10.22–4.98 0.358 was associated with steeper increases in basal area, AGB and density of
Total species richness (R2 = 0.44)
adult trees (Table 2). At 10 years, sites with P content below 4 mg dm−3
Intercept 2.46 2.27–2.65 < 0.001 had a basal area of 13 m2 ha−1, AGB of 42 Mg ha−1 and 291 trees ha−1,
Age 0.19 0.06–0.32 < 0.001 while sites with P content above 4 mg dm−3 had a basal area of
Annual precipitation 0.19 0.09–0.30 < 0.001 24 m2 ha−1, AGB of 137 Mg ha−1 and 1243 trees ha−1 (Fig. 2). Canopy
Base saturation −0.01 −0.15–0.06 0.381
height increased faster in the early years with soil base saturation
Forest cover 0.02 −0.04–0.17 0.242
Correction factor 2.33 1.36–3.30 < 0.001 (Table 2; Fig. 2). The canopy frequently closed (80%) in the first few
years but this was variable, especially for sites with higher annual
Richness of non-planted species (R2 = 0.65)
Intercept −0.19 −0.62–0.24 0.040 precipitation (> 1628 mm year−1). Annual precipitation above
Age 1.02 0.64–1.40 < 0.001 1660 mm was related to higher sapling density at younger sites, leading
Phosphorus −0.31 −0.71–−0.02 < 0.001 to fast initial growth and higher total and non-planted species richness.
The vegetation attributes of direct-seeded sites were in the same

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M.G. Freitas, et al. Forest Ecology and Management 438 (2019) 224–232

Fig. 2. Structural attributes of the vegetation community in sites restored by direct seeding (blue and red dots), seedling planting (black dots), and natural re-
generation (green dots) in a 10-year chronosequence in Mato Grosso, Brazil. Dots represent the sites sampled. Regression curves describe the trajectories of each
vegetation attribute over time. For the vegetation attributes affected by environmental variables other than age, different regressions are presented for sites with
different levels of these variables (high in blue and low in red). The second most important variable other than age was indicated by the size of the dot (see methods
section). Soil P = Phosphorus Content (mg dm−3); Base Sat. = Base Saturation (%); Precipitation = Annual Precipitation (mm year−1); Sand = Percentage of Sand
(%). *Species richness in 500 m2 for trees, 100 m2 for saplings and 25 m2 for seedlings. Dots representing seedling plantings are not shown in the graph of non-planted
species richness because there was no information on what species were planted. Equations for regressions curves are in Table A.1.

229
M.G. Freitas, et al.
range of natural regeneration sites, considering 7–10 y old sites. Both
methods had higher seedling density than seedling plantation (F = 4.0;
DF = 31; P = 0.028; Tukey post hoc comparison). Directed seeded sites
had higher sapling density than seedling planting sites (F = 12.6;
DF = 31; P < 0.001; Tukey post hoc comparison). The other vegetation
attributes did not differ among the three restoration methods.
4. Discussion
Some studies recommend the use of direct seeding for restoration
due to its low cost (Campos-Filho et al., 2013; Engel and Parrotta, 2001;
Palma and Laurance, 2015) and ecological advantages, especially the
high initial seedling density, similar to that of resilient early secondary
forests (Campos-Filho et al., 2013; Meli et al., 2017; Sovu et al., 2010).
We confirmed the ecological effectiveness of direct seeding for tropical
forest restoration based on 72 sites across the spectrum of environ-
mental variation, including high- and moderate-success sites, within a
period of 10 years. Restored sites formed a stratified forest with a closed
canopy that was starting to be colonized by non-planted species, thus
concluding the trigger phase of restoration. Although the values for
vegetation attributes were higher in most direct seeded than natural
regeneration sites, the means were not significantly different. This is
due in part to the high within-treatment variance and the small number
of natural regeneration sites. Seedling and sapling densities were higher
in the direct seeding than in seedling planting sites. It should be noted
that direct seeding and seedling planting were applied in sites with low
potential for natural regeneration while natural regeneration was
mostly allowed to take place in sites with high potential for natural
regeneration.
Direct-seeded sites reached an average of 4200 seedlings ha−1 in
three years, four times the seedling density of seedling planting sites of
the same age in the seasonal semideciduous forests of São Paulo state
(1042 ind ha−1) (Brancalion et al., 2016). The basal area of 10-year-old
sites with soil P content < 4.5 mg dm−3 (13 m2 ha−1) was similar to
the basal area of secondary succession sites in the Amazon at similar
latitudes and with a high potential for natural regeneration (Peña-
Claros, 2003). Sites with soil P content > 4.5 mg dm−3 had a much
higher estimated basal area (24 m2 ha−1). Thus, direct-seeded sites
stored a significant amount of carbon. Considering sites with low soil P
content, a biomass of 4.92 Mg ha−1 year−1 corresponds to an annual
net carbon absorption of 2.46 Mg C ha−1 year−1, similar to the ab-
sorption rate of secondary wet forests ranging in age from 5 to 15 years
(2.35 Mg C ha−1 year−1; Rozendaal et al., 2017) and of neotropical
forests after 20 years of regeneration since the last farming activity
(3.05 Mg C ha−1 year−1; Poorter et al., 2016). Furthermore, before
restoration the sites investigated in this study had been dominated by
exotic grasses, with no natural regeneration (Durigan et al. 2013). The
recognition of direct seeding as a successful method for carbon se-
questration could promote its use and advance the achievement of
national forest restoration goals (Holl and Zahawi, 2014; Poorter et al.,
2016).
Aside from knowing if a restoration method works, we must un-
derstand how this method shapes the trajectory of the developing ve-
getation community (Shoo et al., 2016). For instance, the objective of
planting seedlings that mix rows of pioneer species with rows of high
diversity of species is to establish a canopy within the first two to four
years, shade out invasive grasses, and improve the conditions for the
establishment of late successional species (Rodrigues et al., 2011,
2009). In some cases, however, tree seedlings and saplings are absent
due to the simultaneous growth of planted seedlings, which form a
dense and homogenous canopy, coupled with continuous grass control
for the first few years and soil preparation limited to the seedling
planting spots, creating poor establishment conditions for seeds that
disperse into the area. Thus, both enrichment with late successional
species and canopy management are needed eventually. In contrast, in
areas with high potential for natural regeneration, the unassisted
230
Forest Ecology and Management 438 (2019) 224–232
natural regeneration method leads to a varied vegetation structure re-
sulting from heterogeneity within the site, such as patches of different
soil types, varying densities of invasive species, and random timing of
species colonization, all of which promote forest stratification. In some
cases, however, natural regeneration leads to the formation of a
monodominant canopy that may be transient and densely shaded,
especially in areas with a high potential for natural regeneration
(Chazdon and Uriarte, 2016; Mesquita et al., 2015). Lastly, in the direct
seeding method the seeds are sown in high densities (30 tree seeds
m−2) and include many species and functional groups, resulting in a
stratified forest with a high density of individuals. Trees have a high
height-to-diameter ratio and do not bifurcate in the first years, quickly
forming a tall secondary forest. In these areas, the canopy closes rapidly
(> 80% in seven years) and the density of seedlings and saplings in-
creases, reaching more than 10,000 seedlings and saplings ha−1 in six
years due to the high density of seeds planted. Species richness in-
creases during the first few years as late successional species grow and
enter new sampling classes.
In the present study, non-planted species were able to colonize the
restored areas. We found no relationship between the surrounding
forest cover and the arrival of new species, despite a range in forest
cover proportions of 0 to 65% (mean 18%). Rocha et al. (2016), in a
study of natural regeneration of abandoned pastures in southwestern
Amazonia, did not find any influence of the surrounding forest within a
120 m radius buffer on species arrival. They attributed this result to two
possible causes: first, most species in tropical regions have limited seed
dispersal, with seeds spreading only a few meters from the edge of the
forest (Howe et al., 2010); second, the species that were able to colonize
regenerating areas were dispersed by bats, which were able to disperse
seeds for kilometers. Our studied sites were only 10 years old, a rela-
tively short period to observe the influence of landscape on species
colonization (Holl et al., 2017). However, the richness of non-planted
species was higher in sites with both higher precipitation and lower
fertility. One possibility is that higher soil fertility caused faster canopy
closure and basal area increment, which could result in insufficient
light for seedling establishment of light-demanding species (Capers
et al., 2005; Dupuy & Chazdon, 2006; Dupuy & Chazdon, 2008).
The vegetation had higher structural development in sites with
higher soil fertility. Basal area and aboveground biomass were higher in
sites that had high soil P content. In addition, both aboveground bio-
mass and tree height increased with soil base saturation. Phosphorus
constrains tree growth in highly degraded and leached tropical soils and
is correlated with productivity in old-growth Amazon forests (Quesada
et al., 2012). Soil and leaf phosphorus are important in defining the
photosynthetic capacity of tropical forests (Bahar et al., 2017). More-
over, tropical tree distributions may be limited by soil phosphorus
content, because many species have pronounced associations with ei-
ther high or low phosphorus content (Condit et al., 2013). In our study,
the great variation in phosphorus content is explained by the previous
use of the soil. Sites with higher phosphorus content had been used for
grain production, with the application of limestone and annual fertili-
zation of the soil, which resulted in higher tree growth rates. Thus,
fertilization could be used before direct seeding to accelerate tree de-
velopment. Annual precipitation was less important for forest devel-
opment than soil fertility, which is not surprising since the annual
precipitation only ranged from 1519 to 1957 mm.
Our results show a high variability in the rate of vegetation recovery
following direct seeding, due to the measured, and possibly other not
measured, environmental conditions, which is an inherent source of
variation in any study. An advantage of direct seeding is the possibility
of performing a quick evaluation of the initial results; the density of
established seedlings in direct-seeded sites can be assessed a few
months after planting (Meli et al., 2017). In sites with low numbers of
species, enrichment with seedlings is a possibility, using slow-growing
species or species that failed to establish through direct seeding. In sites
where the grass cover is high and tree seedling density is also high,
M.G. Freitas, et al. Forest Ecology and Management 438 (2019) 224–232

exotic grasses must be controlled (Grossnickle and Ivetić, 2017). One
option for that is selective herbicide use, but the application must be
directed towards the tussocks and must happen only after seeded spe-
cies have established (Campos-Filho et al., 2013). Keeping these re-
commendations in mind, direct seeding is an efficient tropical forest
restoration method to attain vegetation attributes that trigger the suc-
cessional process and promote a structure that is more similar to re-
silient natural regeneration sites than to sites where seedlings have
been planted.
Acknowledgements
This work was funded by the Rufford Small Grants Foundation,
PROEX/CAPES (Project No. 1789/2015) and the Graduate Program in
Ecology at University of Brasília, Instituto Socioambiental, Associação
Rede de Sementes do Xingu, and Embrapa Genetic Resources and
Biotechnology. We are thankful to the Brazilian Ministry of Education
for funding MGF and SBC’s M.Sc. fellowship via CAPES and CNPq. We
heartily thank Cleber Marcelino for fieldwork assistance. Barbara
Zimbres, Leticia Gomes, Catarina Jokovac, Luisa Carvalheiro and André
Coutinho contributed with ideas for this study.

Appendix A

Table A.1
Equations for regressions curves showed in Fig. 2.
Vegetation attributes Equation N R2 P

Basal area (Soil P ≤ 4.5 mg) Y = 1.28x + 0.22 63 0.44 < 0.001
Basal area (Soil P > 4.5 mg) Y = 2.74x − 2.91 9 0.77 0.001
Aboveground biomass (Soil P ≤ 4.5 mg) Y = 4.92x − 6.56 63 0.44 < 0.001
Aboveground biomass (Soil P > 4.5 mg) Y = 10.96x − 16.81 9 0.74 0.002
Canopy cover (Precipitation ≤ 1607 mm) Y = 38.12log(x) + 5.67 29 0.67 < 0.001
Canopy height (Base Saturation ≤ 17%) Y = 3.16log(x) + 0.80 31 0.69 < 0.001
Canopy height (Base Saturation > 17%) Y = 3.10log(x) + 1.27 41 0.15 0.007
Tree density (Soil P ≤ 4.5 mg) Y =37.38x − 48.20 63 0.31 < 0.001
Tree density (Soil P > 4.5 mg) Y = 87.74x − 164.64 9 0.70 0.003
Sapling density (Precipitation ≤ 1694 mm) Y = 3798log(x) – 95 32 0.34 < 0.001
Total species richness (Precipitation ≤ 1694 mm) Y = 5.33log(x) + 6.06 32 0.31 < 0.001
Non-planted species richness (Precipitation ≤ 1694 mm) Y = 0.25x − 0.48 32 0.20 0.006
Non-planted species richness (Precipitation ≤ 1694 mm) Y = 0.54x − 0.57 40 0.09 0.032

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