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Animal-dispersed pioneer trees enhance the

early regeneration in Atlantic Forest
restoration plantations
ARTICLE in NATUREZA & CONSERVAC~AO REVISTA BRASILEIRA DE CONSERVAC~AO DA NATUREZA MAY 2015
Impact Factor: 1.33 DOI: 10.1016/j.ncon.2015.03.005

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6 AUTHORS, INCLUDING:
Ricardo Viani

Diana Carolina Vsquez Castro

Universidade Federal de So Carlos

University of So Paulo

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Natureza & Conservao

Brazilian Journal of Nature Conservation
Supported by Boticrio Group Foundation for Nature Protection
http://www.naturezaeconservacao.com.br

Research Letter

Animal-dispersed pioneer trees enhance the early

regeneration in Atlantic Forest restoration
plantations

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Q1

Ricardo Augusto Gorne Viani a, , Natassia Bonini Vidas b , Mariana Meireles Pardi b ,
Diana Carolina Vsquez Castro b , Eduardo Gusson b , Pedro H.S. Brancalion b
a

Laboratrio de Silvicultura e Pesquisas Florestais, Departamento de Biotecnologia e Produco Vegetal e Animal, Universidade Federal de
So Carlos (UFSCar), Araras, SP, Brazil
b Departamento de Cincias Florestais, Escola Superior de Agricultura Luiz de Queiroz (ESALQ), Universidade de So Paulo (USP),
Piracicaba, SP, Brazil

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a r t i c l e

i n f o

a b s t r a c t

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Article history:

Planting of native trees has been adopted in many tropical regions worldwide as a central

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Received 1 March 2014

forest restoration method, but little is known concerning the role that these planted species

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Accepted 13 March 2015

play in catalyzing forest regeneration beneath their canopies. We investigated the role of

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Available online xxx

animal-dispersed tree species in catalyzing the regeneration of woody species in the understory of restoration plantings. We assessed both the density and richness of tree seedlings

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Keywords:

within plots located beneath the canopy of both animal-dispersed and abiotic-dispersed

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Frugivores

tree species planted in three riparian forest restoration sites with ages of five, six and eight

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Natural regeneration

years. The proportion of animal-dispersed tree seedlings increased with plantation age.

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Restoration ecology

The richness of animal-dispersed tree seedlings was higher beneath animal-dispersed trees

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Seed dispersion

in the eight-year-old planting. The density of animal-dispersed tree seedlings was higher

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Tropical forest restoration

under animal-dispersed trees when sites were analyzed altogether. The top three species
in regeneration density beneath the canopy were animal-dispersed trees, and from the top
ten, seven were animal-dispersed species. We suggest that animal-dispersed pioneer trees
which facilitate natural regeneration and promote a high density and richness of woody
species beneath their canopies should be considered as framework species for tropical
forest restoration.
2015 Associaco Brasileira de Cincia Ecolgica e Conservaco. Published by Elsevier
Editora Ltda. All rights reserved.

Corresponding author.
E-mail address: ragviani@yahoo.com.br (R.A.G. Viani).
http://dx.doi.org/10.1016/j.ncon.2015.03.005
1679-0073/ 2015 Associaco Brasileira de Cincia Ecolgica e Conservaco. Published by Elsevier Editora Ltda. All rights reserved.

Please cite this article in press as: Viani, R.A.G., et al., Animal-dispersed pioneer trees enhance the early regeneration in Atlantic Forest restoration
NCON 27 16
plantations. Nat Conservacao. 2015. http://dx.doi.org/10.1016/j.ncon.2015.03.005

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Introduction
Historical land uses in many human-modified tropical
landscapes have compromised the resilience of natural
ecosystems, and thus hampered their potential for self27
28
recovery after abandonment (Chazdon, 2003). In order to
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recreate the conditions necessary for secondary succession in
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such a scenario, active restoration is needed to help overcome
31
limitations concerning seed-dispersal and micro-site conditions (Holl and Aide, 2011). The planting of native trees has
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thus been adopted in many tropical regions worldwide as one
of the main methods for restoring agricultural lands in this
34
35
context (Rodrigues et al., 2011). Little is known however about
36
the role that the species used in those plantings play in cat37
alyzing forest regeneration beneath their canopies. Assessing
38
the differing performances of planted tree species in permit39
ting the spontaneous regeneration of other native species
40
is thus a key tool for improving the ecological efficiency of
41
restoration plantings.
42
Different approaches have been adopted toward the selec43
tion of tree species. They are usually based on the assumed
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functional role of the species in recovering degraded lands,
45
and follow classifications such as: pioneer and non-pioneer
46Q2 species, filling and diversity species (Rodrigues et al., 2009),
47
nurse plants (Padilla and Pugnaire, 2006), and framework
48
species (Blakesley et al., 2002). Most of these approaches
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have focused on the reestablishment of a forest struc50
ture that is able to facilitate succession, but the role
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of such species in enhancing seed arrival remains little
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studied.
53
The reintroduction of animal-dispersed tree species in
54
degraded lands may be particularly important for forest
55
restoration in highly fragmented landscapes, since they can
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contribute to overcome dispersal limitation by attracting seed
57
dispersers that may bring in their guts seeds they have con58
sumed nearby (Lindell et al., 2012). However, animal-dispersed
59
species do not form a homogeneous functional group, and
60
may contain species with a distinct ability to attract fru61
givorous birds and bats to restoration sites, as a result of
62
fruiting phenology, and fruit yield, size, nutritional value,
63
smell and color (Wunderle, 1997). Consequently, outcomes
64
for plant regeneration in restoration sites can differ widely
65
amongst animal-dispersed species, and the identification and
66
utilization of plant species that are more attractive to frugi67
vores may enhance restoration success. An assessment of the
68
regeneration community beneath the canopy of planted tree
69
species may thus be useful for indicating which species should
70
be favored in restoration plantings (Wydhayagarn et al., 2009).
71
In this sense, we sought to investigate the role of animal72
dispersed tree species in catalyzing the regeneration of woody
73
species in the understory of restoration plantings. We aimed to
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answer the following questions: (1) is the richness and density
75
of animal-dispersed tree seedlings higher under the canopy
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of animal-dispersed planted trees than under the canopy
77
of abiotic-dispersed ones? (2) Is the regeneration of exotic
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animal-dispersed species higher under the canopy of animal79
dispersed planted species? (3) Which planted tree species have
80
a higher density of animal-dispersed tree seedlings under
81
their canopies?
25

Material and methods

Study sites

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The study was carried in Piracicaba, So Paulo State, southeastern Brazil, in a region originally covered by Seasonally
Tropical Dry Forest, within the Atlantic Forest biome (22 42 S,
47 37 W; altitude: 546 m; climate: Cwa, Koeppens system).
The study sites exist within a highly fragmented landscape
with less than 10% forest cover that is principally a matrix of
sugar-cane fields and urban zones. We selected three riparian forest restoration plantings with ages of five, six and eight
years; the first two sites were previously occupied by pastures
of the African grasses Urochloa spp., and the eight-year-old
site by annual crops. Restoration planting was carried out in
all sites using approximately 80 native tree species, which
were planted in a 3 2 m spacing scheme (1.667 seedlings per
ha) and stimulated by the control of exotic grasses (usually
Urochloa spp. and Panicum maximum) via mechanical mowing
and herbicide application. Bird communities in these plantings are dominated by generalist species, typical of disturbed
sites (Alexandrino et al., 2013).

Data collecting
We counted and identified to species every tree seedling taller
than 10 cm present in 2 3 m plots, these plots being located
under the canopy of both animal-dispersed and abioticdispersed trees planted in each restoration site. The trunk
of the tree was located at the center of each plot. We classified each surveyed tree seedling into three categories, each
category consisting of two classes: species origin (native or
exotic), colonizing status (local or immigrant) and dispersal
syndrome (animal-dispersed or abiotic-dispersed species). We
considered as native the seedlings belonging to species that
are known to occur naturally in the study region and as exotic
all those belonging to species that do not naturally occur in
the study region. We classified as local the seedlings belonging to planted species and as immigrant those that do not
belong to any of the tree species planted at the specific restoration site where the seedling was surveyed. To better explore
the results when performing analyses, we created new categories by combining two or three of the seedling categories
previously mentioned.
We evaluated 215 planted trees, amounting to 86, 74 and 55
trees at the five, six and eight-year old sites respectively. Altogether, we assessed natural regeneration under the canopy of
21 planted tree species (four to six animal-dispersed species,
and four to seven abiotic-dispersed species per restoration
site), including pioneers and non-pioneers (Table S1). All field
data was collected in July 2011.

Data analysis
We calculated tree seedling species richness and density
under the canopy of planted trees, in terms of the absolute and proportional values according to the total number of
tree seedlings. These calculations were performed separately
for each restoration site and for each of the three seedling

Please cite this article in press as: Viani, R.A.G., et al., Animal-dispersed pioneer trees enhance the early regeneration in Atlantic Forest restoration
NCON 27 16
plantations. Nat Conservacao. 2015. http://dx.doi.org/10.1016/j.ncon.2015.03.005

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trees planted in the restoration sites. In all cases, we employed

a p critical value of 0.05.

We found 94 different woody species under the canopy of

the planted trees, 76 of these being native ones. The majority
of tree seedlings belonged to immigrant, native and animaldispersed species (Table 1). Altogether, we surveyed 2593
individual seedlings under the canopies of 215 planted trees
(2.01 plants m2 ); with 70.3% of these seedlings belonging to
animal-dispersed species and 45.5% of them being animaldispersed seedlings of immigrant species. The proportion of
animal-dispersed and abiotic-dispersed tree seedlings varied
according to plantation age (2 = 39.01; df = 2; p < 0.001), with
an increase in the proportion of animal-dispersed with planting age (from five to six years old 2 = 17.33; df = 1 and p < 0.001;
from six to eight years old 2 = 4.23; df = 1 and p = 0.04) (Table 1).
A similar pattern of variation in the proportion of animaldispersed seedlings with plantation age was found when only
immigrant species were included in the analysis (2 = 23.39;
df = 2 and p < 0.001). In this case, we found a higher proportion
of animal-dispersed seedlings within the eight-year-old site in
comparison to the younger restoration sites (from five to eight
years old 2 = 19.18; df = 1 and p < 0.001; from six to eight years
old 2 = 19.17; df = 1 and p < 0.001).

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0

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Number of planted tress (samples)

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Number of planted tress (samples)

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Results

Number of animal-dispersed species

in the natural regeneration

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categories described above (origin, colonizing status and dispersal syndrome).

We used the non-parametric chi-square test to compare the proportions of animal-dispersed abiotic-dispersed,
local immigrant, and native exotic tree seedlings among
restoration planting ages. These analyses were undertaken to
infer whether there was a notable change in the tree seedling
community according to the age of the restoration planting.
To compare the richness of animal-dispersed seedlings
under the canopy of animal-dispersed and abiotic-dispersed
planted trees we generated rarefaction curves, and this
was due to the fact that in all restoration sites the proportion of planted trees investigated varied between the
two dispersal syndromes. Rarefaction curves were obtained
with 1000 simulations, separately for each site, using the
EcoSim software (Entsminger, 2012). To compare the density
of animal-dispersed tree seedlings under animal-dispersed
versus abiotic-dispersed planted trees for each restoration
planting age, and also the density of native and exotic
animal-dispersed immigrant seedlings under the canopy of
animal-dispersed versus abiotic-dispersed planted trees, we
performed an unpaired Students t-test. Finally, we calculated
the density of animal-dispersed plants beneath the canopy
of each planted species and presented the results graphically according to a rank of regeneration density. For all of
the analyses described in this paragraph, we considered only
tree seedlings belonging to immigrant (non-planted) species in
order to avoid including plants that could have originated from

Number of animal-dispersed species

in the natural regeneration

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Number of animal-dispersed species

in the natural regeneration

134

15

20

25

30

Number of planted tress (samples)

Fig. 1 Number of animal-dispersed tree species under the canopy of abiotic-dispersed (dashed line) and animal-dispersed
(continuous line) planted trees in 5 (A), 6 (B) and 8-years-old forest restoration plantings (C). Only seedlings of immigrant
(non-planted) native species were accounted. Rarefaction curves were obtained with 1000 simulations. Vertical bars
represent the 95% confidence intervals.
Please cite this article in press as: Viani, R.A.G., et al., Animal-dispersed pioneer trees enhance the early regeneration in Atlantic Forest restoration
NCON 27 16
plantations. Nat Conservacao. 2015. http://dx.doi.org/10.1016/j.ncon.2015.03.005

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Table 1 Richness and density of the tree seedling community regenerating in five, six and eight years old restoration
plantings (Piracicaba-SP, Southeastern Brazil). Values between parentheses are the percentage of total number of species
or density in each restoration planting.
Group

Identity
Total
185
186
187
188
189
190
191
192
193
194
195
196
197
198
199
200
201
202
203
204
205
206
207
208
209
210
211
212
213
214
215
216
217
218

5y

6y

8y

19 (35%)
35 (65%)
32 (59%)
22 (41%)
9 (17%)
45 (83%)
58 (100%)

25 (43%)
33 (57%)
32 (55%)
26 (45%)
14 (24%)
44 (76%)
61 (100%)

22 (36%)
39 (64%)
34 (56%)
27 (44%)
8 (13%)
53 (87%)
223 (100%)

The proportion of local and immigrant tree seedlings varied among restoration sites (2 = 91.01; df = 2; p < 0.001). We
found a higher proportion of immigrant species in the eightyear-old site (from five to eight years old 2 = 86.28; df = 1
and p < 0.001; from six to eight years old 2 = 59.11; df = 1 and
p < 0.001) (Table 1).
Estimated richness for the tree seedling community did not
significantly differ between dispersal syndromes within the
two younger restoration sites (Fig. 1A and B). There was however a tendency of higher richness of animal-dispersed species
in the eight-year-old plantation, revealed after the sample of
25 planted trees (Fig. 1C). The density of animal-dispersed
tree seedlings did not differ between planted trees dispersal
syndromes for each individual age, but it was higher under
animal-dispersed trees when sites were analyzed altogether
(Fig. 2A).
We found 18 exotic tree species present under the canopy of
the planted trees, six animal- and 12 abiotic-dispersed species.
Although the density of native tree seedlings was higher under
the canopy of animal-dispersed trees, we found no difference
in the density of exotic animal-dispersed immigrant seedlings
connected to the dispersal syndrome (animal-dispersed or
abiotic-dispersed) of the planted tree (Fig. 2B). In addition, the
proportion of native and exotic seedlings under the canopy
did not differ between animal- and abiotic-dispersed planted
trees (2 = 0.035; df = 1 and p = 0.8524).
The mean regeneration density of animal-dispersed
species under the canopy of the planted species varied from
3095 plants ha1 for Luehea divaricata (wind dispersed) up
to 16,429 plants ha1 for Trema micrantha (animal dispersed),
giving rise to a variation of 530% in the regeneration density. The top three species in regeneration density were
animal-dispersed trees, and from the top ten, seven were
animal-dispersed species (Fig. 3).

Discussion
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Despite only evaluating relatively young restoration plantings immersed in a highly fragmented landscape, we found
high richness and density of animal-dispersed immigrant tree
species regenerating under the planted trees. These restoration plantations thus appear to be actively functioning as
successful catalysts of natural regeneration in degraded areas
situated within a region assumed to contain strong limitations to dispersal, as indicated by the high establishment of
immigrant animal-dispersed species from adjacent areas to

5y
0.80 (36%)
1.44 (64%)
1.07 (48%)
1.17 (52%)
0.67 (30%)
1.57 (70%)
1.92 (100%)

6y

8y

0.52 (27%)
1.40 (73%)
0.98 (51%)
0.94 (49%)
0.44 (23%)
1.48 (77%)
1.78 (100%)

0.39 (22%)
1.39 (78%)
1.27 (71%)
0.52 (29%)
0.35 (20%)
1.43 (80%)

A
Animal-dispersed seedlings in the natural
regeneration (plants.m-2)

Origin

Abiotic-dispersed
Animal-dispersed
Immigrant species
Local species
Exotic
Native
54 (100%)

Seedling density (plants m2 )

a
1.6
b

1.2

0.8

0.4

0.0
5

AII

Restoration planting age (years)

B
Animal-dispersed seedlings in the natural
regeneration (plants.ha-1)

Dispersal syndrome

Species richness

10 000

8000

6000

4000

2000

Exotic species

Native species

Fig. 2 Mean regeneration density (standard error) of

animal-dispersed seedlings in forest restoration plantings
of different ages (A) and of exotic and native
animal-dispersed species (B) under the canopy of
animal-dispersed (light gray) and abiotic-dispersed trees
(dark gray) in Atlantic Forest restoration plantings,
Piracicaba, southeastern Brazil. Only immigrant species
(non-planted ones) were accounted. Bars followed by
different letters significantly differ in the density of
animal-dispersed seedlings (Students t-test, p < 0.05).

the forest restoration sites. Since most of the species and

individuals regenerating under the canopy of the trees in the
restoration plantations belonged to immigrant (non-planted)
species, our results suggest that in a relative short period of

Please cite this article in press as: Viani, R.A.G., et al., Animal-dispersed pioneer trees enhance the early regeneration in Atlantic Forest restoration
NCON 27 16
plantations. Nat Conservacao. 2015. http://dx.doi.org/10.1016/j.ncon.2015.03.005

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Animal-dispersed seedlings ubder the

canopy (plants.ha-1)

16 000
14 000
12 000
10 000
8000
6000
4000
2000

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nt
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fo
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ity

Fig. 3 Mean regeneration density of animal-dispersed species under the canopy of animal-dispersed (dark gray) and
non-animal-dispersed trees (light gray), in Atlantic Forest restoration plantings, Piracicaba, southeastern Brazil. Only
seedlings of immigrant (non-planted) species were accounted.

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time, the composition of the plant community under restoration will be considerably transformed from the planted one.
Furthermore, our results show that the planted tree species do
not have, at least during the initial years after planting, a major
role as seed and seedling sources for forest regeneration.
Higher natural regeneration richness under animaldispersed trees in the eight-year-old site and the similarity
between the two younger restoration sites may be a consequence of an increase in fruit abundance in the older site.
This increase may be due to a greater fruit yield and/or number of animal-dispersed trees that matured to the reproductive
stage in the older site, whilst in the younger plantations fruit
production must not have yet been sufficient to produce a
difference in the performance of animal-dispersed trees in
comparison to the abiotic-dispersed sites (Wunderle, 1997).
Although initially attracted into restoration zones by animaldispersed trees, frugivores do not disperse seeds only under
those trees (Wunderle, 1997); they may use any kind of tree
as feeding or resting perches, dispersing seeds via defecation
and regurgitation. Indeed, we did find a relatively high density and richness of animal-dispersed seedlings regenerating
beneath the canopies of abiotic-dispersed trees. Additionally,
the majority of potential seed dispersers found in the restoration sites studied is not strictly frugivores (Alexandrino et al.,
2013) and may use any type of tree for foraging insects and
other food sources, thus defecating or regurgitating seeds
throughout the forest.
These seed dispersers typical of disturbed areas
could also be playing an undesirable role in disseminating
animal-dispersed exotic species. However, we did not find
that exotic tree seedlings are more abundant under animaldispersed trees than abiotic-dispersed, neither did we find any

difference in the proportion of exotic and native tree seedlings

connected to the dispersal syndrome of the planted trees.
Therefore, in comparison with native trees, exotic ones are
not particularly likely to be favored under the canopy of
animal-dispersed trees. Nevertheless, it remains necessary to
improve our understanding of the interaction between fauna
and animal-dispersed exotic trees in order to prevent future
biological invasion processes, and all of the subsequent costs
that the management of exotic species in forest restoration
sites entails (Buchley et al., 2006).
In spite of the overall patterns observed for animaland abiotic-dispersed trees, great variation existed amongst
species performance in catalyzing the understory regeneration. We found great variation in the density of tree seedlings
under the canopies of the 21 investigated species. This is consistent with other studies (Fink et al., 2009) and was in fact
expected since there is significant variation in the traits of
animal-dispersed tree species concerning frugivore attraction;
for example fruit color, smell, size and phenology (Wunderle,
1997). A key category of species that help to facilitate the
regeneration of woody species are animal-dispersed pioneer
trees. Pioneer trees are frequently used in tropical forest
restoration plantations (Souza and Batista, 2004; Rodrigues
et al., 2011) as they grow fast and tolerate competition with
invasive grasses (Campoe et al., 2014). Due to the importance
of fauna on catalyzing regeneration in forest restoration plantings, we suggest that the potential to attract seed-dispersing
animals be a key criterion in the selection of tree species for
forest restoration projects. Following from this conclusion,
we recommend animal-dispersed pioneer trees be used as
framework species for tropical forest restoration (Blakesley
et al., 2002).

Please cite this article in press as: Viani, R.A.G., et al., Animal-dispersed pioneer trees enhance the early regeneration in Atlantic Forest restoration
NCON 27 16
plantations. Nat Conservacao. 2015. http://dx.doi.org/10.1016/j.ncon.2015.03.005

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Concluding remarks and further advances

We conclude that animal-dispersed trees, especially pioneers,
enhance early regeneration in the studied forest restoration
sites. We suggest they should be considered top priorities for
tropical forest restoration. In addition, we recommend further studies to address knowledge gaps regarding the role
that seed dispersal plays in catalyzing secondary succession
in forest restoration plantings. Firstly, it is important to better
investigate which animals consume the fruits of each planted
tree species, so that restoration practitioners may select tree
species that are especially attractive to seed dispersers (Lindell
et al., 2012). In addition, research concerning the reproductive
phenology of trees within restoration sites should be pursued
and should relate to the supply of resources to animals.

Conflicts of interest
310

The authors declare no conflicts of interest.

Appendix A. Supplementary data

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Supplementary data associated with this article can be found,

in the online version, at doi:10.1016/j.ncon.2015.03.005.

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references
314

315
316
317
318
319
320
321
322
323
324
325
326

Alexandrino, E.R., et al., 2013. Aves do campus Luiz de Queiroz

(Piracicaba, SP) da Universidade de So Paulo: mais de 10 anos
de observaces neste ambiente antrpico. Atualidades
Ornitolgicas 173, 4052.
Blakesley, D., et al., 2002. Research needs for restoring tropical
forests in Southeast Asia for wildlife conservation: framework
species selection and seed propagation. New For. 24, 165174,
http://dx.doi.org/10.1023/A:1021311700220.
Buchley, Y.M., et al., 2006. Management of plant invasions
mediated by frugivore interactions. J. Appl. Ecol. 43, 848857,
http://dx.doi.org/10.1111/j.1365-2664.2006.01210.x.
Campoe, O.C., et al., 2014. Atlantic forest tree species responses
to silvicultural practices in a degraded pasture restoration

plantation: from leaf physiology to survival and initial growth.

For. Ecol. Manage. 313, 233242,
http://dx.doi.org/10.1016/j.foreco.2013.11.016.
Chazdon, R.L., 2003. Tropical forest recovery: legacies of human
impact and natural disturbances. Perspectives in Plant
Ecology. Evol. Syst. 6, 5171,
http://dx.doi.org/10.1078/1433-8319-00042.
Entsminger, G.L., 2012. EcoSim Professional: Null Modeling
Software for Ecologists. Version 1. Acquired Intelligence Inc.,
Kesey-Bear, & Pinyon Publishing, Montrose, CO.
Fink, R.D., et al., 2009. Patch size and tree species influence the
number and duration of bird visits in forest restoration plots
in southern Costa Rica. Restor. Ecol. 17, 479486,
http://dx.doi.org/10.1111/j.1526-100X.2008.00383.x.
Holl, K.D., Aide, T.M., 2011. When and where to actively restore
ecosystems? For. Ecol. Manage. 261, 15581563,
http://dx.doi.org/10.1016/j.foreco.2010.07.004.
Lindell, C.A., et al., 2012. Migratory bird species in young tropical
forest restoration sites: effects of vegetation height, planting
design, and season. Bird Conserv. Int. 22, 94105,
http://dx.doi.org/10.1017/S0959270911000177.
Padilla, F.M., Pugnaire, F.I., 2006. The role of nurse plants in the
restoration of degraded environments. Front. Ecol. Environ. 4,
196202, http://dx.doi.org/10.1890/1540-9295
(2006)004[0196:TRONPI2.0.CO;2].
Rodrigues, R.R., et al., 2009. On the restoration of high diversity
forests: 30 years of experiences in the Brazilian Atlantic
Forest. Biol. Conserv. 142, 12421251,
http://dx.doi.org/10.1016/j.biocon.2008.12.008.
Rodrigues, R.R., et al., 2011. Large-scale ecological restoration of
high-diversity tropical forests in SE Brazil. For. Ecol. Manage.
261, 16051613, http://dx.doi.org/10.1016/j.foreco.2010.07.005.
Souza, F.M., Batista, J.L.F., 2004. Restoration of seasonal
semideciduous forests in Brazil: influence of age and
restoration design on forest structure. For. Ecol. Manage. 191,
185200, http://dx.doi.org/10.1016/j.foreco.2003.12.006.
Wunderle Jr., J.M., 1997. The role of animal seed dispersal in
accelerating native forest regeneration on degraded tropical
lands. For. Ecol. Manage. 99, 223235,
http://dx.doi.org/10.1016/S0378-1127(97)00208-9.
Wydhayagarn, C., et al., 2009. Bird communities and seedling
recruitment in restoring seasonally dry forest using the
framework species method in Northern Thailand. New
Forests 38, 8197, http://dx.doi.org/10.1007/s11056-009-9133-z.

Please cite this article in press as: Viani, R.A.G., et al., Animal-dispersed pioneer trees enhance the early regeneration in Atlantic Forest restoration
NCON 27 16
plantations. Nat Conservacao. 2015. http://dx.doi.org/10.1016/j.ncon.2015.03.005

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