“Cerrado” restoration by direct seeding: field establishment and initial growth of 75 trees, shrubs and grass species

Abstract

The coexistence of grasses, herbs, shrubs and trees characterizes savannas; therefore, to restore such ecosystems one should consider re-introducing all these growth forms. Currently, little is known about field establishment of most “Cerrado” (Brazilian savanna) species that could be used for restoration purposes. Most knowledge on restoration is focused on planting seedlings of tree species from forest physiognomies. Alternatively, direct seeding can be an appropriate method to re-introduce plants of different life forms to restore savannas. We evaluated the initial establishment success under field conditions of 75 “Cerrado” native species (50 trees, 13 shrubs, and 12 grasses) in direct seeding experiments in four sites in Central Brazil for 2.5 years. For that, we tagged and measured tree and larger shrub species and estimated ground cover by small shrub and grass species. Sixty-two species became established (42 trees, 11 shrubs and 9 grasses) under field conditions. Thirty-eight of the 48 tagged species had relatively high emergence rates (>10%) and 41 had high seedling survival (>60%) in the first year. Among grasses and small shrub species, Andropogon fastigiatus Sw., Aristida riparia Trin., Schizachyrium sanguineum (Retz.) Alston, Lepidaploa aurea (Mart. ex DC.) H.Rob., Stylosanthes capitata Vogel, S. macrocephala M.B.Ferreira & Sousa Costa, Achyrocline satureioides (Lam.) DC. and Trachypogon spicatus (L.f.) Kuntze had the greatest initial establishment success (up to 30% soil cover). The data on harvesting period, processing mode and field establishment for these 75 species can be readily used in restoration efforts in the “Cerrado”.

Full text

ORIGINAL ARTICLE
‘‘Cerrado’’ restoration by direct seeding: field establishment
and initial growth of 75 trees, shrubs and grass species
Keiko Fueta Pellizzaro
1,2
•Alba O. O. Cordeiro
3
•Monique Alves
1
•
Camila P. Motta
1
•Gustavo M. Rezende
1
•Raissa R. P. Silva
4
•Jose
´Felipe Ribeiro
5
•
Alexandre B. Sampaio
6
•Daniel L. M. Vieira
1,7
•Isabel B. Schmidt
1
Received: 11 October 2016 / Accepted: 14 February 2017
Botanical Society of Sao Paulo 2017
Abstract The coexistence of grasses, herbs, shrubs and
trees characterizes savannas; therefore, to restore such
ecosystems one should consider re-introducing all these
growth forms. Currently, little is known about field
establishment of most ‘‘Cerrado’’ (Brazilian savanna)
species that could be used for restoration purposes. Most
knowledge on restoration is focused on planting seedlings
of tree species from forest physiognomies. Alternatively,
direct seeding can be an appropriate method to re-introduce
plants of different life forms to restore savannas. We
evaluated the initial establishment success under field
conditions of 75 ‘‘Cerrado’’ native species (50 trees, 13
shrubs, and 12 grasses) in direct seeding experiments in
four sites in Central Brazil for 2.5 years. For that, we
tagged and measured tree and larger shrub species and
estimated ground cover by small shrub and grass species.
Sixty-two species became established (42 trees, 11 shrubs
and 9 grasses) under field conditions. Thirty-eight of the 48
tagged species had relatively high emergence rates ([10%)
and 41 had high seedling survival ([60%) in the first year.
Among grasses and small shrub species, Andropogon
fastigiatus Sw., Aristida riparia Trin., Schizachyrium san-
guineum (Retz.) Alston, Lepidaploa aurea (Mart. ex DC.)
H.Rob., Stylosanthes capitata Vogel, S. macrocephala
M.B.Ferreira & Sousa Costa, Achyrocline satureioides
(Lam.) DC. and Trachypogon spicatus (L.f.) Kuntze had
the greatest initial establishment success (up to 30% soil
cover). The data on harvesting period, processing mode
and field establishment for these 75 species can be readily
used in restoration efforts in the ‘‘Cerrado’’.
Keywords Direct sowing Ecological restoration 
Grassland restoration Herbaceous layer Neotropical
savanna
Electronic supplementary material The online version of this
article (doi:10.1007/s40415-017-0371-6) contains supplementary
material, which is available to authorized users.
&Keiko Fueta Pellizzaro
keiko.pellizzaro@icmbio.gov.br; keikofueta@gmail.com
1
Programa de Po
´s-Graduac¸a
˜o em Ecologia, Universidade de
Brası
´lia - UnB, Instituto de Biologia, Campus Darcy Ribeiro,
Brası
´lia, Distrito Federal 70919-970, Brasil
2
Instituto Chico Mendes de Conservac¸a
˜o da Biodiversidade -
ICMBio, Reserva Biolo
´gica da Contagem, Rod. DF 003 Via
EPIA km 8,5, Brası
´lia, Distrito Federal 70635-800, Brasil
3
Programa de Po
´s-Graduac¸a
˜o em Bota
ˆnica, Universidade de
Brası
´lia - UnB, Instituto de Biologia, Campus Darcy Ribeiro,
Brası
´lia, Distrito Federal 70919-970, Brasil
4
Programa de Po
´s graduac¸a
˜o em Cie
ˆncias Florestais, UnB -
Fac. de Tecnologia - Secretaria de Po
´s-Graduac¸a
˜oem
Cie
ˆncias Florestais, Campus Universita
´rio Darcy Ribeiro,
Brası
´lia, Distrito Federal 70910-900, Brasil
5
Embrapa Cerrados, Empresa Brasileira de Pesquisa
Agropecua
´ria - Embrapa, Rodovia BR-020, Km 18 Caixa
Postal: 08223, Planaltina, DF 73310-970, Brasil
6
Centro Nacional de Pesquisa e Conservac¸a
˜oda
Biodiversidade do Cerrado e Caatinga, CECAT/ICMBio,
EQSW 103/104, Bloco ‘‘C’’, Setor Sudoeste, Brası
´lia,
DF 70670-350, Brasil
7
Embrapa Recursos Gene
´ticos e Biotecnologia -
CENARGEN, Parque Estac¸a
˜o Biolo
´gica, PqEB, Av. W5
Norte (final) Caixa Postal 02372, Brasilia, DF 70770-917,
Brasil
123
Braz. J. Bot
DOI 10.1007/s40415-017-0371-6

Introduction
Savannas are naturally dominated by an herbaceous layer
with tree density varying according to soil and climate
conditions and fire regime, among other factors (Higgins
et al. 2000). Therefore, ecological restoration of such areas
must consider the original vegetation structure in order to
actually contribute to conservation of biodiversity and
ecosystem services (Chazdon 2008; Veldman et al. 2015a).
Nevertheless, because most restoration studies are focused
on forest ecosystems, restoration recommendations in both
scientific and practical arenas are mostly focused on tree
planting (Ruiz-Jaen and Aide 2005; Rodrigues et al. 2009).
Afforestation or equivocal restoration threaten savanna and
grassland ecosystems by decreasing endemic plant and
animal diversity, decreasing ground water recharge and
increasing aboveground biomass allocation, which increa-
ses susceptibility to fire events (Veldman et al. 2015b).
The dominance of exotic invasive species is a frequent
challenge for restoring degraded ecosystems (Durigan et al.
2013; Holl et al. 2014). This is especially true in tropical
savannas and grasslands, which are commonly dominated
by invasive grasses (Williams and Baruch 2000). Invasive
grass species reduce light and water availability (Levine
et al. 2003); intensify fire regimes (D’Antonio and Vitou-
sek 1992); and alter other ecosystem features (Chapin et al.
2000). Most grass species are shade-intolerant and can be
eliminated by fast-growing forest trees in restoration areas,
as long as fire and other disturbances are excluded (Cabin
et al. 2002). However, planting fast-growing tree species
that could outcompete these invasive grasses might not be
possible or appropriate to restore grassland and savanna
ecosystems (Veldman et al. 2015b). Besides, the seedlings
from most native savanna tree species are slow-growing
due to higher investment in below-ground tissues (De
Castro and Kauffman 1998), which allows for survival
during the dry season. In addition, native herbaceous and
shrub species are important parts of open ecosystems
structure, function and diversity (Mendonc¸a et al. 2008;
Bond and Parr 2010). Therefore, to effectively restore
savanna and grassland environments, it is essential to select
and use herbaceous and shrub species that can establish and
compete with invasive grasses, without excluding slow-
growing tree species.
The ‘‘Cerrado’’ phytogeographical domain, in Central
Brazil, is a biodiversity hotspot due to its high levels of
endemism and high rates of conversion of native vegetation
(da Silva and Bates 2002). It is the most biodiverse savanna
region in the world, where millions hectares are targeted to
be restored by federal legislation (Brasil 2000; Soares Filho
et al. 2014). To effectively restore such vast areas, it is
urgent to improve knowledge on restoration ecology, and
the first step should be generating information on species
propagation and establishment in field conditions. There
are more than 12,000 plant species native from the ‘‘Cer-
rado’’ domain, many of which are endemic, and about 6000
are herbaceous (Ratter et al. 1997; Mendonc¸a et al. 2008).
Tree species diversity is high, especially in riparian forests,
whereas herbs and shrubs represent 87% of the flora in the
grassland and savanna physiognomies (Mendonc¸a et al.
2008), which originally covered around 70% of the ‘‘Cer-
rado’’ domain (Sano et al. 2007). Native species from
‘‘Cerrado’’ grassland and savanna physiognomies, hereafter
referred as ‘‘Cerrado’’, were rarely tested for field estab-
lishment (Silva et al. 2015), and very little is known about
the use of herbaceous species for restoration in the
Brazilian savanna (see Filgueiras and Fagg 2008; Aires
et al. 2014). In the Federal District of Brazil, forest trees
are often used to restore areas originally covered by
‘‘Cerrado’’, due to their faster growth rates, higher seed
production and availability on nurseries (de Sousa 2015).
This practice is also widespread across savanna ecosystems
in the rest of Brazil.
Low-cost and effective methods are desirable for large-
scale restoration (Holl and Aide 2011; Campos Filho et al.
2013). Direct seeding is a relatively low-cost restoration
technique that allows for the introduction of different plant
growth forms simultaneously. While it is commonly
applied worldwide in open ecosystems such as grasslands
(Palma and Laurance 2015), restoration of savanna
ecosystems in Brazil through direct seeding is still rare
(Silva et al. 2015) and grassland restoration is almost
nonexistent (Overbeck et al. 2013).
In this study, we aimed to investigate the establishment
success in field conditions of a large number of species, of
different growth forms, that could potentially be used in
restoration experiments and practice. We present results of
seedling emergence in both greenhouse and field condi-
tions, as well as seedling survival in the field for 75 species
(50 tree species, 13 shrubs and 12 grasses) native to
‘‘Cerrado’’ up to 2.5 years after seeding. Our results pro-
vide important information for species selection in
restoration efforts in ‘‘Cerrado’’ areas.
Methods
Study sites – We evaluated the establishment success of 75
species seeded in seven restoration experiments in four
sites in Central Brazil. Three study sites were located in the
Federal District: (1) A
´gua Limpa Experimental Farm of
University of Brası
´lia (155605500S, 475600300 W); (2)
Contagem Biological Reserve (153805800 S, 475105300 W);
(3) Entre Rios Farm (155703000S, 472702600 W), a private
K. F. Pellizzaro et al.
123

farm. Site 4, Chapada dos Veadeiros National Park
(140700300S, 473803100 W), is located in the state of Goia
´s
(Table 1).
All study sites were originally ‘‘Cerrado’’ sensu stricto
areas that were converted to pasture. Only site 2 was used
for mechanized agriculture, but it was colonized by exotic
pasture grasses after abandonment. The study region is
within a tropical savanna climate, with dry winters and
rainy summers (Aw Ko
¨ppen); the mean temperature is
21 C, and average precipitation is 1500 mm (90% of
which is concentrated from October to May; INMET
2009). Mean precipitation in the four study sites is similar
(Table 1).
Soils are latosols in sites 1, 2 and 4 and cambisols in site
3. All sites were dominated by invasive grass species (more
than 98% soil cover), with very low density of native plants
(\1 individual, on average, per 10 m
2
plot). Agricultural
activities in all areas had been terminated before the start of
restoration experiments. The most common invasive
grasses in study sites are also common invaders throughout
Brazil and other tropical areas (Zenni and Ziller 2011):
Urochloa decumbens (Stapf) R.D. Webster, Urochloa
humidicola (Rendle) Morrone & Zuloaga, Urochloa
brizantha (Hochst. ex A. Rich.) R.D. Webster, Andropogon
gayanus Kunth, Melinis minutiflora P. Beauv. and Hy-
parhenia rufa (Nees) Stapf.
Experimental design – Direct seeding experiments
were carried out from 2011 to 2014 according to the study
sites (detailed in Table 1). We collected seeds/propagules
used in the direct seeding experiments from areas around
the restoration sites in the 8 months preceding the sowing,
according to species phenology. We processed propagules
according to each species features (detailed in Table 2).
For species with seeds larger than 0.3 cm, we selected and
eliminated visually unviable seeds (predated, aborted). We
stored seeds in paper bags in fresh (room temperature) and
dry conditions until sowing. No pre-treatment to break seed
dormancy was applied before seeding, except for Annona
crassiflora Mart. seeds, which were soaked in a gibberellin
acid solution (1 g of GA3, 200 mL of alcohol and 1 L of
water) for 48 h. We also used Stylosanthes spp. seeds sold
commercially (S. capitata and S. macrocephala), Campo
Grande variety.
At all sites, soil was plowed one or two times during the
dry season (May–October) prior to seeding to decrease
dominance by invasive grasses and soil compaction. We
carried out direct seeding manually at the beginning of the
rainy season (late October–early December) following
three field experiment types: sowing beds (6 91.2 m);
sowing rows (30 m linear meters); and broadcast sowing in
whole plots (20 920 m), according to year and experi-
mental site (Table 1). We buried hard, large, round-seeded
species (C0.5 cm diameter) by lightly plowing soil after
seeding, whereas flat and smaller seeds were seeded after
plowing on the soil surface (Table 2).
In sowing rows and beds, we planted one tree seed every
20 cm (one seed m
-1
species
-1
). In seed-broadcasting
plots, we sowed 25–34 tree seeds m
-2
along with a mix of
grass and shrub species in high density (4–16 species; seed
density varying from 5 to 1100 viable seeds m
-2
species
-1
;
Table 3). We chose this relatively high seed density to
maximize the chances of promoting fast ground cover by
native species and preventing the reestablishment and
dominance of invasive grasses.
Data collection – To characterize seedling emergence
during the first rainy season, we sampled experimental
areas 3 and 6 months after sowing (which corresponds to
the middle and the end of the first rainy season). To
evaluate survival of woody species and ground cover of
herbaceous species, we sampled the experimental areas
every 6 months up to 2.5 years, which corresponds to the
end of the second rainy season after seeding.
We tagged all seedlings from the 50 tree species and from
eight of the shrub species in planting rows and beds, and
measured their height (soil to apical bud) every 6 months. To
sample seed-broadcasting experiments, we established two
10 m
2
(20 90.5 m) subplots within each 400 m
2
experi-
mental plot. We estimated ground cover of native grasses and
shrubs sowed by using the line-point intercept method
(Herrick et al. 2009), sampling 200 points along a 20-m line
Table 1 Study sites, experimental and restoration areas through direct seeding of 75 savanna species in Central Brazil
Site Altitude
(m)
Annual rainfall
(mm)
Year of
seeding
Soil type Restoration total
area (m
2
)
Experimental design Experimental
area
Sampled
area
1 1080 1460 2011
a
Latosol 486 54 96m91.2 m beds 389 m
2
389 m
2
2 1100 1668 2012
a
Latosol 30,000 36 930 m rows 1080 m 1080 m
2013 29,000 6 920 m 920 m plots 2400 m
2
120 m
2
3 1060 1350 2013 Cambisol 2400 6 920 m 920 m plots 2400 m
2
120 m
2
4 1240 1453 2012
a
Latosol 30,000 15 910 m 9100 m plots 15,000 m
2
135 m
2
2013 30,000 12 920 m 920 m plots 4800 m
2
240 m
2
2014 30,000 18 920 m 920 m plots 7200 m
2
360 m
2
a
We controlled weeds only on areas sown in 2011 and 2012 by manual weeding and/or mechanized mowing between beds, rows and plots
‘‘Cerrado’’ restoration by direct seeding: field establishment and initial growth of 75 trees, shrubs…
123

Table 2 Growth form; seed collection time; processing mode (removing pulp device ‘‘RPD,’’ sieve, grass shredder machine ‘‘GSM,’’ manual
separation ‘‘MS’’); field planting mode (buried ‘‘B,’’ or not buried ‘‘NB’’); mean mass of 100 seeds ±SD (values without SD were measured
only once); number of seeds tested in green house (GH) in each year (Y); mean percentage seedling emergence in greenhouse (GHE) ±SD
(values without SD were tested only once—1 year) of Brazilian savanna native species
Species Family Growth
form
Seed
collection
Processing
mode
Planting
mode
100 seeds (g) # Seeds
GH: Y1;
Y2; Y3
GHE (%)
Grass species
Andropogon bicornis
L.
Poaceae Herb May GSM NB 0.23 300; 100 5.5 ±6.0
Andropogon
fastigiatus Sw.
Poaceae Herb June GSM NB 0.11 ±0.01 4000 0.0
Andropogon sp. Poaceae Herb July GSM NB 0.02 300; 200 19.0 ±25.5
Aristida riparia Trin Poaceae Herb May GSM NB 0.12 ±0.02 100; 100;
200
10.5 ±0.9
Aristida aff. riparia. Poaceae Herb June GSM NB 0.15 ±0.03 100; 4000 1.5 ±2.1
Aristida sp1 Poaceae Herb May GSM NB 0.15 ±0.02 100 35.0
Axonopus aureus
P.Beauv.
Poaceae Herb May Sieve NB 0.06 ±0.01 na na
Axonopus pellitus
(Nees ex Trin.)
Hitchc. & Chase
Poaceae Herb May GSM NB 0.012 ±0.008 (b) 100 4.0
Echinolaena inflexa
(Poir.) Chase
Poaceae Herb May Sieve NB 0.22 ±0.04 100 17.0
Loudetiopsis
chrysothrix (Nees)
Conert
Poaceae Herb June GSM NB 0.47 ±0.05 4000 13.0
Schizachyrium
sanguineum (Retz.)
Alston
Poaceae Herb June GSM NB 0.19 ±0.05 100; 4000 3.5 ±0.7
Trachypogon
spicatus (L.f.)
Kuntze
Poaceae Herb June GSM NB 0.24 100; 4000 2.5 ±3.54
Shrub species
Anacardium humile
A. St.-Hil.
Anacardiaceae Shrub September–
October
MS B 238.39 ±7.60 100; 100 63.0 ±43.8
Achyrocline
satureioides (Lam.)
DC.
Asteraceae Shrub August–
September
GSM NB 0.05 ±0.00 100 4.0
Aldama bracteata
(Gardner)
E.E.Schill. &
Panero
Asteraceae Shrub April–May GSM NB 0.15 ±0.04 100; 100 48.3 ±27.1
Lepidaploa aurea
(Mart. ex DC.)
H.Rob.
Asteraceae Shrub June– GSM NB 0.08 ±0.03 100; 100 10.5 ±0.7
Vernonanthura
phosphorica (Vell.)
H.Rob.
Asteraceae Shrub August GSM NB 0.03 ±0.00 100 10.0
Jacaranda ulei
Bureau &
K.Schum.
Bignoniaceae Shrub August Sieve NB 2.70 (a) 100 8.0
Zeyheria montana
Mart.
Bignoniaceae Shrub August Sieve NB 6.67 100 7.0
Parinari obtusifolia
Hook.f.
Chrysobalanaceae Shrub October RPD B 206.00 100 0.0
K. F. Pellizzaro et al.
123

Table 2 continued
Species Family Growth
form
Seed
collection
Processing
mode
Planting
mode
100 seeds (g) # Seeds
GH: Y1;
Y2; Y3
GHE (%)
Bauhinia cf dumosa
Benth.
Fabaceae Shrub October Sieve B 372.00 ±114.00 100 5.0 ±4.2
Mimosa claussenii
Benth.
Fabaceae Shrub September GSM B 3.16 ±0.55 100; 100;
100
22.6 ±12.4
Mimosa sp. Fabaceae Shrub August Sieve B 0.93 ±0.11 100 0.0
Senna alata (L.)
Roxb.
Fabaceae Shrub June Sieve B 5.50 ±0.28 100; 100 13.0 ±9.5
Stylosanthes capitata
Vogel ?S.
macrocephala
M.B. Ferreira &
Sousa Costa
a
Fabaceae Shrub na na NB 0.27 ±0.01 100; 100 23.3 ±4.6
Tree species
Anacardium
occidentale L.
Anacardiaceae Tree September–
October
MS N 448.43 na na
Astronium
fraxinifolium
Schott
Anacardiaceae Tree September Sieve B 5.66 ±0.26 100; 100 79.3 ±20.3
Myracrodruon
urundeuva Allema
˜o
Anacardiaceae Tree September Sieve B 1.94 ±1.68 100; 100;
100
44.0 ±49.4
Schinopsis
brasiliensis Engl.
Anacardiaceae Tree August Sieve B 14.72 ±3.23 100; 100 4.5 ±4.9
Annona crassiflora
Mart.
Annonaceae Tree March RPD B 64.95 ±5.95 100; 100;
100
26.0 ±24.0
Aspidosperma
macrocarpon Mart.
Apocynaceae Tree September MS B 85.71 ±3.72 100; 100 40.0 ±32.9
Aspidosperma
tomentosum Mart.
Apocynaceae Tree September MS B 21.6 100 46.0
Hancornia speciosa
Gomes
Apocynaceae Tree October RPD B 23.00 ±1.00 100 63.0
Schefflera
macrocarpa
(Cham. & Schltdl.)
Frodin.
Araliaceae Tree July Sieve B 5.88 (e) 100; 100 20.0 ±24.0
Eremanthus
glomerulatus Less.
Asteraceae Tree September Sieve NB 0.40 ±0.19 200; 100;
100
32.0 ±40.9
Cybistax
antisyphilitica
(Mart.) Mart.
Bignoniaceae Tree October MS NB 1.99 ±0.04 200 49.0
Handroanthus
ochraceus (Cham.)
Mattos
Bignoniaceae Tree September–
October
Sieve NB 1.32 ±0.13 100 93.0
Jacaranda brasiliana
(Lam.) Pers.
Bignoniaceae Tree August MS B 2.73 ±0.15 100; 100;
100
35.3 ±29.9
Tabebuia aurea
(Silva Manso)
Benth. & Hook.f.
ex S.Moore
Bignoniaceae Tree September–
October
Sieve NB 1.43 (a) na na
Tabebuia caraiba
(Mart.) Bureau
Bignoniaceae Tree October MS NB 16.93 ±0.46 100 39.0
Cordia alliodora
(Ruiz & Pav.) Oken
Boraginaceae Tree October Sieve B 7.67 ±0.13 100 27.0
‘‘Cerrado’’ restoration by direct seeding: field establishment and initial growth of 75 trees, shrubs…
123

Table 2 continued
Species Family Growth
form
Seed
collection
Processing
mode
Planting
mode
100 seeds (g) # Seeds
GH: Y1;
Y2; Y3
GHE (%)
Kielmeyera coriacea
Mart. & Zucc.
Calophyllaceae Tree August–
September
MS NB 10.85 ±0.25 100; 100 28.0 ±24.3
Buchenavia sp. Combretaceae Tree September Sun-dried B 95.21 ±0.61 100 0.0
Buchenavia
tomentosa Eichler
Combretaceae Tree September Sun-dried B 113.12 ±10.77 100 30.0
Terminalia argentea
Mart.
Combretaceae Tree September Sieve B 24.96 ±0.37 100 15.0
Terminalia fagifolia
Mart.
Combretaceae Tree September Sieve B 1.82 100 2.0
Davilla elliptica
A.St.-Hil.
Dilleniaceae Tree August GSM/sieve B 3.21 100 0.0
Amburana cearensis
(Allema
˜o) A.C.Sm.
Fabaceae Tree August Sieve B 53.64 100; 100 38.7 ±26.0
Anadenanthera
colubrina (Vell.)
Brenan
Fabaceae Tree August Sieve NB 14.20 ±1.12 100; 100;
100
73.0 ±36.0
Bowdichia
virgilioides Kunth
Fabaceae Tree July MS B 2.12 ±0.02 (c) na na
Copaifera
langsdorffii Desf.
Fabaceae Tree August–
October
Sieve B 100.28 ±9.64 100; 100;
100
44.6 ±32.9
Dalbergia
miscolobium Benth.
Fabaceae Tree September Sieve B 17.42 ±1.51 100 12.0
Dimorphandra mollis
Benth.
Fabaceae Tree June GSM/sieve B 17.62 ±0.37 100 6.0
Dipteryx alata Vogel Fabaceae Tree September None B 2259.06 ±48.47 100;100 32.5 ±44.5
Enterolobium
contortisiliquum
(Vell.) Morong
Fabaceae Tree October GSM/sieve B 45.31 ±0.81 100;100 3.7 ±2.3
Enterolobium
gummiferum
(Mart.) J.F.Macbr.
Fabaceae Tree July–
August
GSM B 51.02 na na
Hymenaea
stigonocarpa Mart.
ex Hayne
Fabaceae Tree September GSM/sieve B 373.07 ±101.86 100; 100;
100
47.5 ±2.4
Machaerium opacum
Vogel
Fabaceae Tree August Sieve NB 61.83 ±38.26 100; 100 3.6 ±3.1
Plathymenia
reticulata Benth.
Fabaceae Tree August Sieve B 4.50 ±0.06 100 22.0
Senegalia polyphylla
(DC.) Britton &
Rose.
Fabaceae Tree July–ago Sieve B 16.41 ±2.01 100; 100 55.7 ±25.5
Stryphnodendron
adstringens (Mart.)
Coville
Fabaceae Tree Ago GSM/sieve B 9.40 ±0.52 100; 200 11.3 ±9.0
Tachigali vulgaris LF
Gomes da Silva &
HC Lima
Fabaceae Tree September Sieve B 22.02 ±0.50 100; 100 44.5 ±16.3
Vatairea macrocarpa
(Benth.) Ducke
Fabaceae Tree September None B 142.86 (g) 100; 200 13.0 ±11.3
Emmotum nitens
(Benth.) Miers
Icacinaceae Tree November None B 142.16 ±34.66(e) na na
K. F. Pellizzaro et al.
123

in each 10 m
2
subplot (one point every 10 cm, 200 points per
subplot) every 6 months. We placed a 2-m-high stick straight
up from the soil at each point and recorded the species
touching the stick at the highest height; points with no plant
species were recorded as bare soil.
Data analyses – We calculated seedling emergence
percentage for 50 trees and eight of the shrub species by
comparing the number of seedlings that emerged in the first
rainy season (May–June) to the number of sowed seeds.
We calculated the survival rates for the first year by
comparing the number of plants surviving 12 months after
sowing to the number of seedlings that emerged. We cal-
culated the survival rate for the second year by comparing
the number of plants still alive after 24 months to the
number that survived the first year.
To verify the germinability of seeds used in field
experiments, we also sowed seeds in a greenhouse simul-
taneously to each of the field experiments, except for the
2011 experiment. We distributed seeds of each species in
plastic trays filled with subsoil lightly covering the seeds
and irrigated daily. We monitored seedling emergence
weekly for 16 weeks. For non-grass species, we planted
100 seeds species
-1
, except for species with low seed
numbers. For grass species, we planted 4000 dias-
pores species
-1
, due to small seed size and low ger-
minability of native grasses (Table 1).
We tested a different group of species in each experi-
ment; there was seeding density variation across experi-
ments due to variations in site, year and seed availability.
We do not intend to compare experiments, sowing methods
Table 2 continued
Species Family Growth
form
Seed
collection
Processing
mode
Planting
mode
100 seeds (g) # Seeds
GH: Y1;
Y2; Y3
GHE (%)
Byrsonima
crassifolia (L.)
Kunth
Malpighiaceae Tree April RPD B 0.29 ±0.01(d) 100; 100 24.7 ±14.4
Cecropia
pachystachya
Tre
´cul
Urticaceae Tree August–
September
MS NB 0.10 ±0.03 100 0.02
Eriotheca pubescens
(Mart. & Zucc.)
Schott & Endl.
Malvaceae Tree July Sieve B 20.78 ±0.48 100 33.5 ±7.8
Guazuma ulmifolia
Lam.
Malvaceae Tree October GSM/sieve B 0.63 100 12.0
Tibouchina
candolleana (Mart.
ex DC.) Cogn.
Melastomataceae Tree September Sieve NB 0.11 ±0.07 200; 100 31.7 ±39.9
Brosimum
gaudichaudii
Tre
´cul
Moraceae Tree October MS B 142.86 na na
Eugenia dysenterica
(Mart.) DC.
Myrtaceae Tree October RPD B 90.97 ±40.42 100; 100 8.0 ±6.9
Alibertia edulis
(Rich.) A.Rich.
Rubiaceae Tree September–
November
Sieve B 0.89 (a) 100 1.0
Magonia pubescens
A. St.-Hil.
Sapindaceae Tree August MS NB 182.32 ±55.15 100; 100;
100
62.0 ±38.0
Solanum lycocarpum
A. St.-Hil.
Solanaceae Tree July–
December
RPD B 2.78 ±0.76 100; 100;
100
23.0 ±20.8
Qualea grandiflora
Mart.
Vochysiaceae Tree October Sieve NB 12.0 ±4.0 (f) na na
(a) Saloma
˜o et al. (2003), (b) Carmona et al. (1999), (c) Gonc
¸alves et al. (2008), (d) Garcı
´a-Nu
´nez et al. (2001), (e) Kuhlmann (2012),
(f) Kutschenko (2009), (g) Mori et al. (2012)
na not available. Species are grouped by life form, listed in alphabetical order by family and species name
a
Campo Grande variety, set of these two species sold commercially, evaluated as a sample
‘‘Cerrado’’ restoration by direct seeding: field establishment and initial growth of 75 trees, shrubs…
123

or even study years; therefore, no comparisons are pre-
sented for such purposes. The central aim of the analyses
presented here is to synthesize information on seed har-
vesting period, processing and field establishment success
of the studied species.
Results
In field conditions, 62 species (42 trees, 11 shrubs and 9
grasses) produced seedlings in the first rainy season after
planting. Of these, 38 (32 trees and six shrubs) had at least
10% emergence in the first rainy season, with 30 of them
(27 trees and three shrubs) reaching at least 20%. After the
first year, 36 trees and five shrubs had above 60% of sur-
vival with 19 of them (17 trees and two shrubs) having
emergence above 20 and [80% survival rate. Anacardium
humile,Enterolobium gummiferum,Anacardium occiden-
tale,Magonia pubescens,Handroanthus ochraceus and
Vatairea macrocarpa were the species with best field
establishment (see Table 4and also Supplementary Mate-
rial 1). The survival of woody individuals between the first
and second year was in general similar to the one observed
during the first year and relatively high for most species
(Table 4).
After the first rainy season (6 months after sowing), tree
seedling height was on average 7.2 ±5.9 cm, and after the
second rainy season (1.5 years after sowing) was
10.14 ±8.2 cm. Tachigali vulgaris,Buchenavia tomen-
tosa,Solanum lycocarpum,Plathymenia reticulata,Ere-
manthus glomerulatus and Hymenaea stigonocarpa were
the fastest growing species (Table 4).
Among the grasses and shrub species evaluated by
ground cover, Andropogon fastigiatus,Aristida riparia,
Schizachyrium sanguineum,Lepidaploa aurea,Stylosan-
thes spp., Achyrocline satureioides and Trachypogon spi-
catus became best established in experimental areas,
covering individually 2–30% of the soil. A. fastigiatus had
the highest ground cover (30%) in the first year after
seeding, whereas other species tended to increase their
ground cover in the second year, especially A. riparia,L.
aurea and S. sanguineum (Supplementary Material 1).
Most grass and small shrub species maintained similar
ground cover between the first and second year after
sowing (Table 3).
Most of the species germinated successfully in the
greenhouse (62 species, Table 1), but nine of those species
did not produce seedlings under field conditions (e.g.,
Byrsonima crassifolia,Cybistax antisyphilitica,A. crassi-
flora). Schefflera macrocarpa had a mean of at least 20%
Table 3 Grass and shrub species used in savanna direct seeding restoration experiments in three sites in Central Brazil
Species Sowing density (g m
-2
) Soil cover after first rainy season Soil cover after second rainy season
Achyrocline satureioides 0.880 0.28 ±0.37 2.12 ±2.88
Aldama bracteata 0.033 0.12 ±0.18 0.16 ±0.19
Andropogon bicornis 0.005 1.43 ±1.02 0.04 ±0.38
Andropogon fastigiatus 0.500 30.24 ±3.79 na
Aristida riparia
a,b
0.100 1.21 ±1.21 2.19 ±4.53
Aristida riparia
a
2.000 2.14 ±3.10 15.06 ±12.08
Axonopus aureus 0.080 1.03 ±1.21 0.47 ±1.41
Axonopus cf. pellitus 0.002 0.00 ±0.00 na
Echinolaena inflexa 0.100 0.75 ±0.67 0.17 ±0.93
Lepidaploa aurea
a
0.900 7.43 ±9.00 6.27 ±9.98
Lepidaploa aurea
a
1.125 6.30 ±4.47 21.25 ±11.93
Loudetiopsis chrysothrix 0.325 0.74 ±0.56 0.20 ±1.82
Schizachyrium sanguineum 0.010 6.89 ±7.73 15.95 ±18.47
Stylosanthes spp.
a
0.060 2.80 ±3.10 1.93 ±4.23
Stylosanthes spp.
a
0.173 4.07 ±3.16 3.77 ±3.07
Trachypogon spicatus 0.875 1.48 ±1.71 2.28 ±6.86
Vernonanthura phosphorica 0.500 0.18 ±0.19 na
Sowing density (mean weight of seeds/m
2
±SD); soil cover (Mean ±SD) after first and second rainy season
na not available
a
Species represented in more than one line were seeded in more than one experiment; each line represents the sowing density and consequent
soil cover of each experiment
b
Aristida sp. and Aristida aff. riparia were also seeded but had low rates of establishment, no flowering in the experimental areas and are not
distinguishable from Aristida riparia in early stages, so data from these species establishment are not presented here
K. F. Pellizzaro et al.
123

Table 4 Tree and shrub species for which seedlings were tagged and measured in four experimental direct seeding restoration sites in Central Brazil
Species NGHE% Field emergence first
rainy season (%)
Survival first year
(%)
Survival second
year (%)
Height first
year (cm)
Height second
year (cm)
b
Height third
year (cm)
b
Shrub species
Anacardium humile
a
2 63.0 ±43.8 83.9 (67.8–100.0) 95.3 (91.1–99.4) 94.0 (91.5–92.3) 7.9 ±6.9 7.9 ±3.7 na
Bauhinia cf. dumosa 1 5.0 ±4.2 23.5 52.6 80.7 (76.9–83.3) 3.1 ±2.5 6.2 ±3.7 na
Jacaranda ulei 2 8.0 0.0 na na na na na
Mimosa claussenii
a
2 22.6 ±12.4 35.4 (0.3–70.6) 81.7 (68.3–95.1) 68.9 (21.4–100.0) 5.8 ±15.4 4.2 ±4.0 5.2 ±9.2
Mimosa sp. 1 0 12.2 69.2 na 2.2 ±2.2 na na
Parinari obtusifolia 1 0 0.0 na na na na na
Senna alata 2 13.0 ±9.5 11.5 (3.7–19.2) 73.7 (67.6–79.7) 37.0 (15–56.3) 11.4 ±10.6 10.0 ±5.0 na
Zeyheria montana 1 7.0 12.6 100.0 na 3.6 ±1.5 na na
Tree species
Alibertia edulis 1 1.0 2.5 66.7 na 4.3 ±1.1 na na
Amburana cearensis 1 38.7 ±26.0 6.9 33.3 na 10.6 ±9.2 10.0 na
Anacardium occidentale
a
1 na 69.6 88.3 na 7.7 ±7.3 8.11 ±3.34 na
Anadenanthera colubrina 4 73.0 ±36.0 36.9 (6.7–71.1) 74.0 (50.0–100.0) 63.3 (25.0–100.0) 6.4 ±4.7 9.0 ±7.2 na
Annona crassiflora
c
3 26.0 ±24.0 0.0 na na na na na
Aspidosperma macrocarpon
a
4 40.0 ±32.9 34.5 (13.3–51.9) 89.6 (65.5–100.0) 80.0 (60.0–100.0) 9.0 ±3.1 10.3 ±4.4 na
Aspidosperma tomentosum 2 46.0 10.0 (6.7–13.3) 100.0 (100.0–100.0) 80.0 (60.0–100.0) 7.8 7.4 na
Astronium fraxinifolium
a
2 79.3 ±20.3 35.7 (0.0–71.4) 84.7 na 10.1 ±5.8 na na
Bowdichia virgilioides 2 na 12.1 (6.7–17.5) 68.8 (37.5–100.0) 55.0 (50.0–60.0) 3.6 ±1.0 6.8 ±2.1 na
Brosimum gaudichaudii
a
1 na 33.8 80.5 na 7.8 ±2.1 8.29 ±2.69 na
Buchenavia sp. 2 0.0 7.2 (6.6–7.8) 61.4 (42.9–80.0) 55.0 (50.0–60.0) 5.3 ±1.9 6.0 ±3.0 na
Buchenavia tomentosa
a
1 30.0 27.8 96.8 86.11 (50.0–100.0) 14.5 ±8.20 23.6 ±12.8 25.4 ±15.1
Byrsonima crassifolia
c
2 24.7 ±14.4 0.0 na na na na na
Cecropia pachystachya 1 0.02 0.0 na na na na na
Copaifera langsdorffii
a
5 44.6 ±32.9 29.0 (17.4–50.3) 81.3 (34.8–100.0) 86.7 (60.0–100.0) 7.3 ±4.1 7.1 ±2.8 na
Cordia alliodora
a
1 27.0 31.7 83.5 na 9.7 ±6.1 na na
Cybistax antisyphilitica
c
2 49.0 0.0 na na na na na
Dalbergia miscolobium 3 12.0 19.4 (2.8–49.3) 77.3 (57.3–100.0) 85.9 (64.7–100.0) 6.3 ±2.7 9.3 ±4.5 na
Davilla elliptica 1 0.0 0.0 na na na na na
Dimorphandra mollis
a
2 6.0 30.8 (8.3–53.3) 80.0 (60.0–100.0) 90.5 (87.5–93.5) 5.4 ±2.3 6.9 ±2.8 na
Dipteryx alata
a
5 32.5 ±44.5 36.5 (12.9–70.1) 93.5 (77.4–100.0) 89.1 (56.3–100.0) 9.3 ±5.4 12.5 ±6.2 12.8 ±2.1
Emmotum nitens
c
1 na 0.8 50.0 na 4.0 ±0.5 7.8 ±3.9 na
Enterolobium contortisiliquum
a
3 3.7 ±2.3 23.9 (5.7–39.2) 89.2 (71.9–100.0) 63.3 (25.0–100.0) 10.7 ±6.3 13.6 ±9.1 19.7 ±3.5
Enterolobium gummiferum
a
1 na 79.6 91.6 63.3 (25.0–100.0) 17.5 ±6.4 17.95 ±5.93 na
Eremanthus glomerulatus 1 32.0 ±40.9 13.2 93.6 43.8 (0–70.0) 6.8 ±6.5 14.4 ±5.3 19.4 ±17.4
‘‘Cerrado’’ restoration by direct seeding: field establishment and initial growth of 75 trees, shrubs…
123

Table 4 continued
Species NGHE% Field emergence first
rainy season (%)
Survival first year
(%)
Survival second
year (%)
Height first
year (cm)
Height second
year (cm)
b
Height third
year (cm)
b
Eriotheca pubescens Endl. 3 33.5 ±7.8 26.4 (15.0–45.9) 76.0 (55.6–100.0) 97.2 (91.7–100.0) 1.7 ±1.0 4.5 ±3.7 na
Eugenia dysenterica
a
4 8.0 ±6.9 38.5 (3.5–69.3) 92.5 (70.0–100.0) 88.9 (66.7–100.0) 5.2 ±3.6 7.0 ±2.7 5.5 ±5.4
Guazuma ulmifolia 2 12.0 0.0 na na na na na
Hancornia speciosa 1 63.0 15.8 36.8 na 6.9 ±1.6 na na
Handroanthus ochraceus 2 93.0 58.1 (17.3–98.9) 70.1 (40.2–100.0) 77.3 (60.0–90.0) 2.0 ±1.7 3.1 ±3.8 na
Hymenaea stigonocarpa
a
5 47.5 ±2.4 45.7 (5.8–83.3) 88.2 (73.3–100.0) 94.4 (83.3–100.0) 16.0 ±8.2 21.2 ±6.0 18.5 ±13.2
Jacaranda brasiliana 4 35.3 ±29.9 23.7 (8.5–37.8) 77.9 (57.1–94.8) 61.2 (0–100.0) 5.3 ±6.9 9.4 ±18.1 6.2 ±4.2
Kielmeyera coriacea 3 28.0 ±24.3 25.8 (5.5–48.1) 61.4 (30.6–83.9) 58.7 (47.4–71.4) 2.7 ±1.9 3.6 ±4.5 na
Machaerium opacum 3 3.6 ±3.1 3.0 (0.6–7.2) 59.9 (20.0–80.0) 75.0 (50.0–100.0) 5.7 ±2.2 10.2 ±4.4 8.7 ±13.4
Magonia pubescens
a
6 62.0 ±38.0 66.8 (34.2–100.0) 95.9 (91.7–100.0) 95.5 (87.5–100.0) 7.5 ±5.0 9.9 ±6.2 13.9 ±4.6
Myracrodruon urundeuva 2 44.0 ±49.4 62.6 76.6 67.2 (43.8–80.0) 3.7 ±1.7 5.8 ±2.5 na
Plathymenia reticulata 2 22.0 8.0 (7.0–8.9) 76.4 (73.7–79.2) 67.6 (42.8–100.0) 6.8 ±3.4 14.6 ±15.1 26.2 ±15.7
Qualea grandiflora 1 na 50.7 71.9 na 8.5 ±2.2 8.00 ±3.04 na
Schefflera macrocarpa 2 20.0 ±24.0 0.0 na na na na na
Schinopsis brasiliensis 1 4.5 ±4.9 1.1 100.0 na 5.3 ±4.6 7.3 ±5.3 na
Senegalia polyphylla 1 55.7 ±25.5 1.0 50.0 na 9.5 na na
Solanum lycocarpum 5 23.0 ±20.8 31.0 (1.3–63.7) 61.6 (20.0–88.0) 54.5 (30.6–69.1) 6.32 ±9.3 15.1 ±14.3 25.7 ±13.3
Stryphnodendron adstringens
a
3 11.3 ±9.0 20.0 (4.2–39.0) 80.0 (40.0–100.0) 77.2 (50.0–100.0) 3.5 ±1.9 4.9 ±2.8 na
Tabebuia aurea S.Moore 1 na 63.7 74.0 na 2.4 ±0.9 2.56 ±1.13 na
Tabebuia caraiba
a
1 39.0 34.2 88.2 na 6.0 ±6.3 na na
Tachigali vulgaris 2 44.5 ±16.3 31.9 (31.3–32.5) 73.0 (58.0–88.0) 60.0 (32.3–83.3) 10.0 ±6.0 36.4 ±16.6 55.3 ±25.5
Terminalia argentea 1 15.0 8.1 90.9 43.9 (20–86.7) 7.8 ±4.7 5.5 ±1.0 8.8 ±1.8
Terminalia fagifolia 1 2.0 0.0 na na na na na
Tibouchina candolleana 2 31.7 ±39.9 4.4 (0.0–8.9) 25.0 na 9.0 na na
Vatairea macrocarpa
a
1 13.0 ±11.3 56.0 98.7 94.8 (88.9–100) 6.9 ±2.4 7.4 ±3.5 na
Number of experiments in which the species was planted (N); mean percentage seedling emergence in greenhouse (GHE) ±SD; mean field seedling emergence on the first rain season (0.5 year
after sowing) (min -max); mean percentage of survival after first and second dry season (1 and 2 year after sowing) [mean (min -max)]; height one, two and third years after sowing
na not available. Data on seedling height in second and third year are limited to seedling ages according to experiments. Some species were only sowed in the 2013 and 2014 experiments;
therefore, data are not available for second/third year old growth
a
High emergence ([20%) and survival ([80%) species
b
Data on seedling height in 2nd and 3rd years are limited to seedling ages according to experiments. Some species were only sowed in the 2013 and 2014 experiments, therefore data is not
available for second/third year old growth
c
1.0-3.0% field emergence after first rainy season
K. F. Pellizzaro et al.
123

seedling emergence in the greenhouse and no emergence in
field conditions. On the other hand, some species failed to
germinate in greenhouse conditions but successfully
established seedlings in the field (e.g., Mimosa sp. and
Buchenavia sp., Table 4). Emergence in both the field and
in greenhouse was in general higher for tree species com-
pared to shrubs and grasses (Table 2).
Discussion
Our results suggest that through direct seeding, it was
possible to promote the establishment, at least for the first
2.5 years, of 62 trees, shrubs and grass species in relatively
large areas of ‘‘Cerrado’’ previously dominated by invasive
grasses. The planting cost per individual seed in direct
seeding restoration programs is low, and low rates of both
emergence and survival rates are considered normal (Palma
and Laurance 2015). Some authors consider a 10% emer-
gence rate an acceptable threshold (Engel and Parrotta
2001; Campos Filho et al. 2013), and this value is near the
mean emergence rate (18%) obtained in most restoration
projects around the world (Palma and Laurance 2015). We
recorded 38 out of 58 woody species with at least a 10%
emergence rate in the field; and identified 19 species with
emergence rates above 20% associated with C80% sur-
vival rate after the first year. These results indicate that
these species can be successfully used in restoration prac-
tices through direct seeding. In addition, even species with
low establishment rates can be useful to help compose the
community, and increase diversity and richness. Some of
them should be included in direct seeding restoration pro-
grams especially when seed collection and storage are not
expensive.
Aside from these species, we can infer that other naturally
abundant native species with high seed production might be
good candidates for use in direct seeding restoration prac-
tice. Our data from greenhouse experiments indicate that
there might be no direct relationship between seedling
emergence in a greenhouse and seedling establishment in
field conditions. This suggests that greenhouse experiments
might not be worth performing in order to select species
suitable to be planted in direct seeding restoration programs.
Some studied species had good field establishment rates, but
low emergence in the greenhouse. In contrast, other species
had high emergence rates in greenhouse conditions, but low
establishment rate in the field. In a greenhouse, seeds can be
sowed in a precise depth, on a flat soil without lumps, pro-
tected from predation, and there is no water shortage.
However, in a greenhouse, high humidity of air and soil may
increase seed infection by pathogens, and environmental
triggers for germination such as thermal and humidity
variations are absent.
We found high values of seedling survival (80%) in the
first 2.5 years, especially when compared to the 62%
average survival of the seedling planting experiments for
restoration identified in a recent review (Palma and Lau-
rance 2015). Survival after the first dry season is a good
parameter for long-term seedling establishment in savan-
nas, where the length of the dry season can be a severe
constraint to seedling survival due to water deficit in upper
soil layers (Oliveira et al. 2005). Seedling survival between
the first and second year was 92% on average for six
‘‘Cerrado’’ tree species in direct seeding experiments (Silva
et al. 2015). For the 24 species for which we had survival
data from the first to second year, survival rates varied
from 54 to 97% (Senna alata and Eriotheca pubescens,
respectively) with a mean of 75%. Seedlings’ tolerance to
drought may also allow these plants to survive extreme
climatic events that might occur due to climate change
(Palma and Laurance 2015). Aside from water deficit
during the dry season, the major causes of sapling death
were probably dry spells during the rainy season (Assad
et al. 1993), competition with invasive grasses, and ant
herbivory.
The slow growth of ‘‘Cerrado’’ tree seedlings observed
here (see also Silva et al. 2015) is partly due to high
investment in below-ground tissues (De Castro and
Kauffman 1998; Hoffmann and Franco 2003). Due to the
slow aboveground growth of savanna tree species, tree
seedlings will be affected by invasive grasses for years.
Also, trees in savannas will not shade the ground enough to
control invasive grasses. Thus, a key strategy for the suc-
cess of restoration in non-forest ecosystems is the intro-
duction of fast-growing herbaceous species, in high
density, that can cover the soil and compete with invasive
grasses (Filgueiras and Fagg 2008; Hulvey and Zavaleta
2012). Although herbaceous species, especially grasses,
tend to have low seed germinability, they mostly have high
seed production. Therefore, seed harvesting can represent a
low-cost strategy in some sites/regions, allowing for high
density of seeding. Our data show that species such as L.
aurea,A. riparia,A. fastigiatus,S. sanguineum,T. spicatus,
Achyrocline satureoides and Stylosanthes spp., grew fast
and showed high proportion of ground cover, and some
species even reproduced in the first rainy season after
planting. These plants may help to structure the commu-
nity, allowing other native species to establish and survive;
they assume a similar role of fast-growing tree species
commonly recommended for restoration and invasive
grasses control in forest ecosystems (Rodrigues et al.
2009). Native shrub and herbs can readily cover the
ground, which can help control invasive grasses by the
temporal priority effect (Young et al. 2001) and can affect
invasive grasses productivity (Corbin and D’Antonio 2004)
and dominance.
‘‘Cerrado’’ restoration by direct seeding: field establishment and initial growth of 75 trees, shrubs…
123

This study presents information on a relatively large
number of species, which represents a great increase in the
otherwise scarce information on ‘‘Cerrado’’ species estab-
lishment in restoration areas, especially for herbaceous and
shrub species. The information on fruiting period, fruit/
seed processing method and field establishment in early
years after sowing for these species can contribute to the
research and practice on ecological restoration of ‘‘Cer-
rado’’ areas. These results inform restoration allowing for
actions that include the use of different growth forms and
species diversity, which might potentially create a complex
native community.
Acknowledgements These experiments were carried out under
ICMBio research permit number 33390-3. We thank several students
from Restaura-‘‘Cerrado’’ research group for assistance; A. Alboy-
adjian for English review; Fundac¸a
˜o Grupo o Botica
´rio de Protec¸a
˜oa
`
Natureza; ICMBio; CNPq (Edital MCT/CNPq/CT-Agro 26/2010);
and Embrapa/CNA partnership of the Projeto Biomas for financial
support.
References
Aires SS, Sato MN, Miranda HS (2014) Seed characterization and
direct sowing of native grass species as a management tool.
Grass Forage Sci 69:470–478
Assad ED, Sano EE, Masumoto R, De Castro LH, Da Silva FAM
(1993) Veranicos Na Regia
˜o Dos Cerrados Brasileiros Frequen-
cia E Probabilidade de Ocorre
ˆncia. Pesqui Agropecu Bras
28:993–1003
Bond WJ, Parr CL (2010) Beyond the forest edge: ecology, diversity
and conservation of the grassy biomes. Biol Conserv
143:2395–2404
Brasil (2000) Lei 9.985, de 18 de Julho de 2000—Sistema Nacional
de Unidades de Conservac¸a
˜o. http://www.planalto.gov.br/ccivil_
03/leis/L9985.htm. Accessed 21 Oct 2016
Cabin RJ et al (2002) Effects of light, alien grass, and native species
additions on Hawaiian dry forest restoration. Ecol Appl
12:1595–1610
Campos Filho EM et al (2013) Mechanized direct-seeding of native
forests in Xingu, Central Brazil. J Sustain Forest 32:702–727
Carmona R, Martins CR, Fa
´vero AP (1999) Caracterı
´sticas de
Sementes de Gramı
´neas Nativas Do Cerrado. Pesqui Agropec
Bras 34:1067–1074
Chapin FS et al (2000) Consequences of CHANGING BIODIVER-
SITY. Nature 405:234–242
Chazdon RL (2008) Beyond deforestation: restoring forests and
ecosystem services on degraded lands. Science 320:1458–1460
Corbin JD, D’Antonio CM (2004) Competition between native
perenial and exotic annual grasses: implications for an historical
invasion. Ecology 85:1273–1283
D’Antonio CM, Vitousek PM (1992) Biological invasions by exotic
grasses, the grass-fire cycle, and global change. Annu Rev Ecol
Syst 23:63–87
da Silva JMC, Bates JM (2002) Biogeographic patterns and conser-
vation in the South American Cerrado: a tropical savanna
hotspot. Bioscience 52:225
De Castro EA, Kauffman JB (1998) Ecosystem structure in the
Brazilian Cerrado: a vegetation gradient of aboveground
biomass, root mass and consumption by fire. J Trop Ecol
14:263–283
de Sousa AP (2015) Avaliac¸a
˜o de Um Programa de Restaurac¸a
˜ode
Uma Bacia Hidrogra
´fica: Execuc¸a
˜o E Envolvimento Dos
Proprieta
´rios. Dissertation, Universidade de Brası
´lia, Brası
´lia
Durigan G, Ivanauskas NM, Zakia MJB, De Abreu RCR (2013)
Control of invasive plants: ecological and socioeconomic criteria
for the decision making process. Nat Conserv 11:23–30
Engel VL, Parrotta JA (2001) An evaluation of direct seeding for
reforestation of degraded lands in Central Sao Paulo State,
Brazil. For Ecol Manag 152:169–181
Filgueiras TS, Fagg WC (2008) Gramineas Nativas Para Recuperac¸a
˜o
de A
´reas Degradadas No Cerrado. In: Felfili CRMA, Sampaio
JM, Correia JC (orgs.) Bases para a recuperac¸a
˜odea
´reas
degradadas na bacia do Sa
˜o Francisco. Centro de Refere
ˆncia em
Conservac¸a
˜o da Natureza de A
´reas degradadas (CRAD),
Brası
´lia, pp. 89–107
Garcı
´a-Nu
´nez C, Azo
´car A, Silva JF (2001) Seed production and soil
seed bank in three evergreen woody species from a neotropical
savanna. J Trop Ecol 17:563–576
Gonc¸alves JVS, Albrecht JMF, Soares TS, Titon M (2008) Caracter-
izac¸a
˜oFı
´sica E Avaliac¸a
˜o Da Pre
´-Embebic¸a
˜o Na Germinac¸a
˜ode
Sementes de Sucupira-preta (Bowdichia virgilioides Kunth).
Cerne Lavras 14:330–334
Herrick JE, Van Zee JW, Havstad KM, Burkett LM, Whitford WG
(2009) Monitoring manual for grassland shrubland and savanna
ecosystems: quick start, vol I. USDA-ARS Jornada Experimental
Range, Las Cruces
Higgins SI, Bond WJ, Trollope WSW, Bondt WJ, Trollopet WSW
(2000) Fire, resprouting and variability: a recipe for grass-tree
coexistence in savanna. J Ecol 88:213–229
Hoffmann WA, Franco AC (2003) Comparative growth analysis of
tropical forest and savanna woody plants using phylogenetically
independent contrasts. J Ecol 91:475–484
Holl KD, Aide TM (2011) When and where to actively restore
ecosystems? For Ecol Manag 261:1558–1563
Holl KD et al (2014) Efficacy of exotic control strategies for restoring
coastal prairie grasses. Weed Sci Soc Am 7:590–598
Hulvey KB, Zavaleta ES (2012) Abundance declines of a native forb
have nonlinear impacts on grassland invasion resistance. Ecology
93:378–388
INMET (2009) Normais Climatolo
´gicas Do Brasil 1961–1990. http://
www.inmet.gov.br/portal/index.php?r=clima/normaisclimatologi
cas. Accessed 21 Oct 2016
Kuhlmann M (2012). Frutos E Sementes Do Cerrado Atrativos Para a
Fauna: Guia de Campo. Col. Christopher W. Fagg. Rede de
Sementes do Cerrado, Brası
´lia
Kutschenko DC (2009) Fenologia E Caracterizac¸a
˜o de Frutos E
Sementes de Um Cerrado Sensu Stricto, Jardim Bota
ˆnico de
Brası
´lia, Distrito Federal, Brasil, Com E
ˆnfase Nas Espe
´cies Com
Sı
´ndrome Ornitoco
´rica. Dissertation, Universidade de Brası
´lia,
Brası
´lia
Levine JM et al (2003) Mechanisms underlying the impacts of exotic
plant invasions. Proc R Soc Lond B Biol Sci 270:775–781
Mendonc¸a RC et al (2008) Flora Vascular Do Bioma Cerrado:
Checklist Com 12.356 Espe
´cies. In: de Almeida SP, Ribeiro JF,
Sano SM (eds) Cerrado: ecologia e flora, vol 2. Embrapa
Informac¸a
˜o Tecnolo
´gica, Brası
´lia, pp 422–442
Mori ES, Pin
˜a-Rodrigues FCM, Ivanauskas NM, Penteado de Freitas,
N, Brancalion PHS, Martins RB (2012) Guia para germinac
¸a
˜ode
100 espe
´cies nativas. In: Martins RB (org) Sementes florestais:
Guia para germinac¸a
˜o de100 espe
´cies nativas. Instituto Reflo-
resta, Sa
˜o Paulo, pp 29–141
Oliveira RS et al (2005) Deep root function in soil water dynamics in
Cerrado savannas of central Brazil. Funct Ecol 19:574–581
K. F. Pellizzaro et al.
123

Overbeck GE et al (2013) Restoration ecology in Brazil—time to step
out of the forest. Nat Conserv 11:92–95
Palma AC, Laurance SGW (2015) A review of the use of direct
seeding and seedling plantings in restoration: what do we know
and where should we go? Appl Veg Sci 18:561–568
Ratter JA, Ribeiro JF, Bridgewater S (1997) The Brazilian Cerrado
vegetation and threats to its biodiversity. Ann Bot Lond
80:223–230
Rodrigues RR, Lima RAF, Gandolfi S, Nave AG (2009) On the
restoration of high diversity forests: 30 years of experience in
the Brazilian Atlantic forest. Biol Conserv 142:1242–1251
Ruiz-Jaen MC, Aide TM (2005) Restoration success: how is it being
measured? Restor Ecol 13:569–577
Saloma
˜o AN et al (2003) Germinac¸a
˜o de Sementes E Produc¸a
˜ode
Mudas de Plantas Do Cerrado. Rede de Sementes do Cerrado,
Brası
´lia
Sano EE, Rosa R, Brito JLS, Ferreira LG (2007) Mapeamento de
cobertura cegetal do bioma Cerrado: estrate
´gias e resultados.
Embrapa Cerrados, Brasilia
Silva RPRP, Oliveira DR, da Rocha GPE, Vieira DLM (2015) Direct
seeding of Brazilian savanna trees: effects of plant cover and
fertilization on seedling establishment and growth. Restor Ecol
23:393–401
Soares Filho B et al (2014) Cracking Brazil’s forest code. Science
344:363–364
Veldman JW et al (2015a) Toward an old-growth concept for
grasslands, savannas, and woodlands. Front Ecol Environ
13:154–162
Veldman JW, Overbeck GE, Negreiros D, Mahy G, Le Stradic S,
Fernandes GW, Durigan G, Buisson E, Putz F, Bond WJ (2015b)
Where tree planting and forest expansion are bad for biodiversity
and ecosystem services. BioSci Adv Access 20:1–8
Williams DG, Baruch Z (2000) African grass invasion in the
Americas: ecosystem consequences and the role of ecophysiol-
ogy. Biol Invasions 2:123–140
Young TP, Chase JM, Huddleston RT (2001) Community succession
and assembly comparing, contrasting and combining paradigms
in the context of ecological restoration. Ecol Restor 19:5–18
Zenni RD, Ziller SR (2011) An overview of invasive plants in Brazil.
Rev Bras Bot 34:431–446
‘‘Cerrado’’ restoration by direct seeding: field establishment and initial growth of 75 trees, shrubs…
123