This research paper aims to study how proximity to a mature forest contributes to the recovery of an abandoned agricultural area located in a semi-arid climate. The researchers monitored seed rain at different distances from the mature forest in the young regenerating forest that had been abandoned for 18 years. They found that seed input from the mature forest contributed to recolonization in the young forest, but 18 years was not enough time for full recovery of all species present in the mature forest. Seed rain decreased with increasing distance from the mature forest. While some species were present in both forests, they differed in fruiting seasons. The young forest contained species not observed in the mature forest. Proximity facilitated but did not guarantee complete reestablishment of the

1. RESEARCH PAPER
Does proximity to a mature forest contribute to the seed
rain and recovery of an abandoned agriculture area
in a semiarid climate?
J. T. Souza1
, E. M. N. Ferraz2
, U. P. Albuquerque3
& E. L. Araujo3
1 Programa de Pos-Graduacß~ao em Bot^anica, Departamento de Biologia, Universidade Federal Rural de Pernambuco, Recife, Pernambuco, Brazil
2 Instituto Federal de Educacß~ao, Ci^encia e Tecnologia de Pernambuco Recife, Recife, Pernambuco, Brazil
3 Departamento de Biologia, Universidade Federal Rural de Pernambuco, Recife, Pernambuco, Brazil
Keywords
Caatinga; fruiting; recolonisation; resprouting;
seed dispersal.
Correspondence
J. T. Souza, Programa de Pos-Graduacß~ao em
Bot^anica, Departamento de Biologia,
Universidade Federal Rural de Pernambuco,
Recife, Pernambuco, Brazil.
E-mail: jeff-thiago@hotmail.com
Editor
J. Arroyo
Received: 2 May 2013; Accepted: 21 Septem-
ber 2013
doi:10.1111/plb.12120
ABSTRACT
Proximity to forests contributes to the recolonisation of anthropogenic-disturbed
areas through seed input. We evaluated the role of proximity to a mature forest in the
recolonisation of an agricultural area that has been abandoned for 18 years and is cur-
rently a young forest. Seed rain was monitored at fixed distances from the mature for-
est. The type of surface recolonisation (germination versus resprouting) and the
reproductive season were measured in both forests. The majority of plants recolonis-
ing the young forest originated from seed germination. Proximity to the mature forest
contributed to the seed rain in the young forest; however, 18 years has not provided
sufficient time for the recolonisation of 80 species present in the mature forest. Some
species shared between forests differed in their fruiting season and seed dispersal. The
seed rain had a total species richness of 56, a total density of 2270 seedsÁmÀ2
ÁyearÀ1
and predominance of self- and wind dispersal. A significant reduction in seed rain
with increasing distance from the mature forest was observed. The young forest con-
tained 35 species not observed in the mature forest, and the floristic similarity
between the two forests was 0.5, indicating that the two forests are floristically dis-
tinct.
INTRODUCTION
Forests throughout the world have been modified by human
actions and are currently fragmented and separated from other
forests by anthropogenic-disturbed areas. For example, in
semiarid climates, many stretches of native forest have been
converted to agropastoral areas (Sanchez-Azofeifa et al. 2005;
Brunet et al. 2012). However, some of these areas have since
been abandoned and allowed to regenerate naturally (Sampaio
et al. 1998; Buisson et al. 2006). Several studies have shown
that the succession process in abandoned areas is influenced by
the proximity of native undisturbed forests (Lopes et al. 2012),
which function as a germplasm bank. This germplasm bank
provides diaspores through seed rain (Wydhayagarn et al.
2009), enabling replacement and reintroduction of species as
part of the successional process of forest recovery.
Other factors also affect the recolonisation of anthropogenic
areas, including the availability of dispersal vectors (Holl
1998; Wydhayagarn et al. 2009), species modes of dispersal
(Zimmerman et al. 2000; Cubi~na Aide 2001), small-scale
spatial variation (Brunet et al. 2012), the type and duration of
land use (Pereira et al. 2003) and plant regrowth capacity
(Lugoa et al. 2004; Levesque et al. 2011a). For example, areas
that have undergone repeated burning regenerate more slowly
and rely more heavily on seed rain than less disturbed areas
(Dungan et al. 2001; Letcher Chazdon 2009). Additionally,
the resprouting of plants accelerates recolonisation as respro-
uted plants produce seeds more rapidly than those originating
from germinating seeds (Figueir^oa et al. 2006; Levesque et al.
2011a).
Over time, the importance of seed input from other areas
(i.e. allochthonous seed rain) to the succession dynamics of
young forest may decrease through the contribution of locally
produced seeds (i.e. autochthonous seed rain; Young et al.
1987), which makes it difficult to assess the contribution of
allochthonous seed rain to forest recovery. Undoubtedly, seed
rain strongly influences forest dynamics because it renews the
soil seed bank (Herrera Garcıa 2009). However, it is still
unknown whether the close proximity of mature forests to
anthropogenic-disturbed areas guarantees the complete re-
establishment of species diversity in semiarid environments.
Furthermore, little is known about either the time required for
this re-establishment to occur or the time required before res-
prouting plants begin contributing to local seed rain. This lack
of information makes it difficult to both understand the role of
mature forests in the recovery of disturbed areas and address
the limiting factors to seed rain in these areas.
Our hypotheses were (i) the proximity of mature forest
enables rapid floristic recovery in areas previously used for
agriculture, and (ii) 18 years of abandonment is sufficient time
for the regeneration (via germination or resprouting) of indi-
viduals and/or populations and for local seed rain, although
the seed rain of some woody species will still originate primarily
from nearby mature forest. We expected that close proximity to
Plant Biology 16 (2014) 748–756 © 2013 German Botanical Society and The Royal Botanical Society of the Netherlands748
Plant Biology ISSN 1435-8603

2. a mature forest would favour recolonisation, but that 18 years
would not be sufficient for complete floristic recovery,
although local seed rain might occur. We also expected that the
contribution of mature forest to the seed rain of the young for-
est would decrease with distance.
Therefore, we sought to characterise and identify the sea-
sonal (dry versus rainy) differences in the seed rain of a former
agricultural area, abandoned for 18 years, lying adjacent to a
mature forest. To do so, we considered the floristic composi-
tion, types of dispersal syndromes and habits of the plants. We
evaluated the contribution of the adjacent mature forest to the
formation of the young forest to answer the following ques-
tions: (i) was 18 years sufficient for the recovery of species rich-
ness and composition in the abandoned area; (ii) does the seed
rain of the woody species in the abandoned area consist of
locally produced seeds or seeds from elsewhere; (iii) does the
local seed rain in the young forest arise via seed germination or
the resprouting of plants; (iv) does the seed rain in the young
forest vary with distance; and (v) does the amount of allochth-
onous seed rain depend on distance from the mature forest?
MATERIAL AND METHODS
Study area and history of use
The study was performed in a dry vegetation area in northeast
Brazil (Fig. 1A), located at the Agronomic Institute of Pernam-
buco (IPA; 8°14′18″ S, 35°55′20″ W) in Caruaru, Pernambuco.
The forest type is deciduous thorn or hypoxerophytic caatinga.
It has a seasonal climate, with average precipitation of
680 mmÁyearÀ1
and a dry season from September to February;
average temperature varies from 19 to 23 °C. The soil is Eutro-
phic Yellow Podzolic, with a sandy-loam texture (Alcoforado-
Filho et al. 2003).
The native vegetation at the experimental station is currently
reduced to an area of ca. 30 ha, which has been conserved for
more than 50 years (and is considered mature forest). It is iso-
lated from other areas of natural vegetation and is surrounded
by experimental crop fields. The mature forest contains 174
species, of which 74 are woody and 100 are herbaceous; how-
ever, an additional 35 species have not been identified to species
level. Mimosaceae, Fabaceae, Caesalpiniaceae, Euphorbiaceae,
Malvaceae, Asteraceae and Poaceae exhibit high species richness
among the species in the mature forest (Araujo et al. 2005; Reis
et al. 2006; Lucena et al. 2007).
In 1994, a 3-ha area on the edge of the mature forest frag-
ment was manually cut for an experiment on prickly pear
(Opuntia ficus-indica Mill.) cultivation. However, not all root
systems were completely removed during this manual cutting,
enabling future resprouting. A strip approximately 3-m wide
between the mature forest and the cultivated area was main-
tained, forming a ‘narrow corridor’ between the areas. No fer-
tiliser was used to prepare the soil. The area was abandoned
after cultivation, and the forest began to regenerate naturally.
After 18 years, the regenerated vegetation has not yet formed a
complete canopy, and contains many clearings, several young
A
B
Fig. 1. A: Study site within caatinga vegetation, Caru-
aru, Pernambuco, Brazil. B: Schematic of the experimen-
tal design used to investigate seed rain in the young
forest.
Plant Biology 16 (2014) 748–756 © 2013 German Botanical Society and The Royal Botanical Society of the Netherlands 749
Souza, Ferraz, Albuquerque Araujo Seed rain of an abandoned agricultural area in a semiarid climate

3. plants and a few surviving Opuntia plants. We therefore refer
to this abandoned agricultural area as ‘the young forest’. In this
area, species richness (116) is considerable: 32 woody species,
84 herbaceous species and 15 taxa unidentified to species level.
Fabaceae, Asteraceae, Malvaceae, Poaceae, Euphorbiaceae,
Mimosaceae and Caesalpiniaceae predominate in the young
forest (Souza 2010; Lopes et al. 2012; Santos et al. 2013).
Experimental design
To evaluate species composition of the seed rain in the young
forest, we established five transects perpendicular to the mature
forest, separated from each other by 15 m (Fig. 1B). Along each
transect, we placed seed traps at 10-m intervals from the mature
forest (10, 20, 30…up to 210 m), yielding 21 traps per transect
and 105 overall. Considering the five transects together, each
10-m interval represented a distance band or distance interval,
totalling 21 parallel bands spanning 210 m from the mature
forest. Thus, each distance interval had five traps.
Each trap consisted of a cylindrical polyethylene bucket of
81-cm circumference (%25-cm diameter) and 30-cm high. The
total seed rain sample area was 5.48 m2
. The height of the traps
was chosen to minimise seed predation, as animals can disturb
low traps and remove seeds (Galetti et al. 2006). The traps
were placed directly on the ground and fixed with wooden
stakes. A layer of grease was applied around the edge of each
trap to prevent access by small invertebrates and subsequent
predation or removal of seeds. Small holes were made in trap
bases to avoid rainwater accumulation and subsequent seed
decay (Zimmerman et al. 2000; Cubi~na Aide 2001).
Traps were emptied once a month over a 1-year period, and
the contents were taken to the laboratory for processing. The
seeds were manually separated from other material, such as
twigs, leaves and other residues. Next, the seeds were identified
and quantified. The number of seeds was expressed as seeds per
m2
. Seeds were identified using specific bibliographies (Kiss-
man 1997; Kissman 1999; Barroso et al. 1999; Kissman Groth
2000; Maia 2004), by consulting the Professor Vasconcelos
Sobrinho (PEUFR) and Dardano de Andrade Lima (IPA) her-
baria, and by comparing seeds that were collected each month
from the mature forest and the young forest. Unidentified
species were considered morphospecies.
To evaluate whether 18 years was sufficient for the recovery
of species richness and composition of the young forest, we
evaluated the floristic similarities of the young forest to the
mature forest. To do so, we monitored two permanent grids
established during previous studies in the young (Lopes et al.
2012) and mature (Alcoforado-Filho et al. 2003; Lucena et al.
2007) forests, and recorded the species identified in each area.
Each grid consisted of 1 ha divided into 100 contiguous
10 9 10-m plots. A species occurrence table was constructed to
include the species observed in the grids and the species
reported in previous studies in the mature forest (Alcoforado-
Filho et al. 2003; Araujo et al. 2005; Reis et al. 2006; Lucena
et al. 2007; Oliveira et al. 2007) and young forest (Lopes et al.
2012; Santos et al. 2013). In addition, morphological character-
istics (Van Der Pijl 1982; Kissman 1997, 1999; Barroso et al.
1999; Kissman Groth 2000) were adopted to classify species
habit (herbaceous or woody – tree and shrub) and dispersal
syndrome: by wind (anemochorous), by animals (zoochorous)
and self-dispersal (autochorous, including ballistic and baroch-
orous dispersal). After 18 years, seed input into the young for-
est can be from locally produced seed (autochthonous seed
rain), seed produced elsewhere (allochthonous seed rain) and,
finally, mixed seed production, i.e. both allochthonous and
autochthonous seed rain (Young et al. 1987; Melo et al. 2006).
To investigate whether the seeds in the young forest origi-
nated from local seed rain or the mature forest, we monitored
the overlap and displacement of the fruiting and dispersal peri-
ods of only those species occurring in both forests. We also
monitored the presence of seeds in the traps. Within the per-
manent grids, we marked 120 plants in the young forest and
129 plants in the mature forest. We selected only individuals of
woody plant species that were most likely adults (i.e. of repro-
ductive age, although not necessarily reproducing at the time
of marking). The number of individuals selected per species
varied due to the size of the adult population in each grid. All
individuals in populations containing less than ten individuals
in each area were marked. Larger populations had only ten
individuals marked in each area to be consistent with several
previous phenological studies of communities (Machado et al.
1997; Ramırez 2002; Torres Galetto 2011). All selected indi-
viduals were monitored monthly for 1 year for fruiting and dis-
persal times, to identify potential locally produced seeds in the
young forest.
In this study, we categorised the following as local (autoch-
thonous) seed rain: seeds from species that either (i) repro-
duced only within the young forest or (ii) that occurred in
both forests but showed displacement in fruiting and dispersal
times, such that seeds were observed in the traps at the same
time of fruiting in the young forest. We categorised allochtho-
nous seed rain as the seeds of species that did not reproduce in
the young forest. Finally, we categorised mixed seed rain as the
seed rain of species present in both forests and exhibiting over-
lapping fruiting and dispersal times coincident with the seeds
in the traps. The origin of seed rain from herbaceous plants
was not evaluated.
To evaluate whether the local seed rain in the young forest
arose from seed germination or the resprouting of plants, we
observed the type of surface recolonisation exhibited by the
marked plants. Some plants in the young forest may have origi-
nated from the regrowth of root systems or from stumps
remaining in the soil when the vegetation was cleared for the
cultivation of Opuntia, enabling earlier seed production. Indi-
viduals without evidence of cuts or resprouting were consid-
ered as originating from seed germination, while those with
such evidence were not.
Data analysis
The Sørensen index was used to determine floristic similarity
between the forests using only those species identified to spe-
cies level. Similarity was calculated using the following two
methods, both of which considered all mature forest species
observed either during the present study or in previous studies
(Alcoforado-Filho et al. 2003; Araujo et al. 2005; Reis et al.
2006; Lucena et al. 2007; Oliveira et al. 2007): (i) all species in
the mature forest were compared to those represented in the
traps (i.e. in the seed rain of the young forest), and (ii) all
species in the mature forest were compared to all young forest
species observed both during the study and mentioned in the
literature (Souza 2010; Lopes et al. 2012; Santos et al. 2013),
Plant Biology 16 (2014) 748–756 © 2013 German Botanical Society and The Royal Botanical Society of the Netherlands750
Seed rain of an abandoned agricultural area in a semiarid climate Souza, Ferraz, Albuquerque Araujo

4. including those species not found in the seed traps of the pres-
ent study. These two similarity indices were adopted to allow
assessment of complete recovery of the floristic young forest.
Seasonal differences in seed density and species richness of the
seed rain were evaluated using the chi-squared (v2
) test (Zar
1996). Variation in species richness, seed density and dispersal
syndrome density across the established distance interval was
evaluated using the Kruskal–Wallis (H) test (Zar 1996). The
effect of distance from the mature forest on the amount of allo-
chthonous seed rain was evaluated using simple linear regression.
We analysed the effects of distance from the mature forest,
season (dry versus rainy), habit (woody versus herbaceous) and
dispersal syndrome (self, wind or animal) on the number of
seeds in the young forest using a general linear model of analysis
of covariance (GLM ANCOVA) with a Gaussian distribution, and
distance from the mature forest as the covariate. For the ANCOVA
(F-test), the assumption of equal variances was verified with Le-
vene’s test. The assumption of independence of the covariate
was also verified. For the other tests, the normality of the data
was verified using the Shapiro–Wilk test (Zar 1996). Statistical
analyses were performed using BIOSTAT 5.0 (Ayres et al. 2007)
and Statistica version 7.0 (StatSoft, Tulsa, OK, USA).
RESULTS
Characterisation of seed rain in the young forest
A total of 56 species were recorded in the seed rain: 16 woody
species, 24 herbaceous species and 16 morphospecies. The total
seed density was 2269.6 seedsÁmÀ2
ÁyearÀ1
. The seed density
was 971.17 seedsÁmÀ2
ÁyearÀ1
for herbaceous species, 1220.25
seedsÁmÀ2
ÁyearÀ1
for woody species and 78.2 seedsÁmÀ2
ÁyearÀ1
for morphospecies (Table S1).
Seed rain differed significantly between the dry and rainy
seasons (v2
= 13.63; P 0.01), with almost twice as many seeds
in the dry season (1511.1 seedsÁmÀ2
per 6-month) than in the
rainy season, concentrated toward the beginning of the season
(September, October and November). Approximately 50% (28)
of species dispersed seeds only during the dry season. Of these,
39% (11) were self-dispersed, 28% (eight) were wind-dispersed
and 32% (nine) were morphospecies. Approximately 11% (six)
of species (two dispersed by wind and four morphospecies) dis-
persed exclusively during the rainy season (Table S1). The
remaining 22 species dispersed seeds in both the rainy and dry
seasons. Of these species, the following dispersed more seeds
during the dry than rainy season: Gomphrena vaga, Guapira laxa,
Mimosa arenosa, Piptadenia stipulacea, Acacia paniculata, Delilia
biflora and Bidens bipinnata. Other species, including Croton
blanchetianus, Urochloa maxima and Pappophorum pappiferum,
dispersed more seeds during the rainy season (Table S1).
The total annual density of dispersed seeds was highest for
self-dispersed species (1357.5 seedsÁmÀ2
), intermediate for wind-
dispersed species (752.5 seedsÁmÀ2
) and least for animal-dispersed
species (81.4 seedsÁmÀ2
). The diaspores from morphospecies
(78.2 seedsÁmÀ2
) did not comprise any syndrome (Table S1).
Of the species identified to species level, 79 (29 woody and
50 herbaceous) of the 139 mature forest species were not
observed in the young forest. Thirty-seven of these 79 species
were self-dispersed (15 woody and 22 herbaceous), 21 were dis-
persed by wind (five woody and 16 herbaceous) and 21 were
dispersed by animals (nine woody and 12 herbaceous). Of the
101 species in the young forest, 41 (six woody and 35 herba-
ceous) were not observed in the mature forest, of which 23
were self-dispersed (three woody and 20 herbaceous), 13 were
dispersed by wind (all herbaceous), and five were dispersed by
animals (three woody and two herbaceous). Only 60 species
(26 woody and 34 herbaceous) were found in both forests.
The floristic similarity between the species composition of
the mature forest and the seed rain in the young forest was
0.27, despite the short distance (3 m) between forests and the
length of time the young forest had been abandoned (18 years).
However, based on the total species composition of the young
forest, for those species identified to species level (including
those absent from the traps), the floristic similarity between the
young and mature forests was 0.5.
Local seed rain and overlap/displacement of seed production
times
Of the 15 woody species represented by presumed adult indi-
viduals in both forests, only two (Commiphora leptophloeos and
Capparis flexuosa) did not fruit during the monitoring period
(Table S2) and yielded no seeds in the traps (Table S1). The 13
remaining woody species included individuals that fruited and
dispersed seeds during the monitoring period (Table S1).
However, four of them (Bauhinia cheilantha, Ziziphus joazeiro,
Myracrodruon urundeuva and Schinopsis brasiliensis) only
fruited in the mature forest, and two of them (M. urundeuva
and S. brasiliensis) were identified from seeds in the traps, indi-
cating allochthonous seed rain. In contrast, two species
(A. paniculata and Cordia trichotoma) only fruited in the young
forest, and their seed rain was local.
The timing of fruiting and seed rain of the C. blanchetianus,
P. stipulacea, Lantana camara and G. laxa populations (Fig. 2)
differed between the two forests. With the exception of
L. camara, the months during which the seeds of the other
three species were found in the traps corresponded only to the
reproductive period of the young forest, indicating that their
seed rain was local. In contrast, Mimosa arenosa, Poincianella
pyramidalis and Anadenathera colubrina (Fig. 2) did not have
different fruiting and seed rain times, suggesting that their seed
rain may be mixed; i.e. comprising seeds produced both locally
and in the mature forest. L. camara also had mixed seed rain,
despite the temporal displacement of its fruiting period.
In addition to the 15 species discussed above, four woody
species were found in the seed rain of the young forest
(Table S1). We identified only young individuals of Sebastiana
jacobinensis in the young forest, indicating that the seed rain
from this species originated from the mature forest (i.e. the
seed rain was allochthonous). Ptilochaeta bahiensis was found
in the traps, but no individuals were in the young forest, indi-
cating that its seed rain also originated from the mature forest.
Lippia cf. alba and Croton rhamnifolius were not found in the
mature forest but were represented by seeds in the traps, indi-
cating that their seed rain was local (Table S1).
Types of surface recolonisation: resprouting of plants versus
seed germination
In the young forest, 22% (26 of 120) of the selected individuals
of the 15 woody species arose from resprouting of cut plants,
and approximately 65% (17) of them produced seeds. The
Plant Biology 16 (2014) 748–756 © 2013 German Botanical Society and The Royal Botanical Society of the Netherlands 751
Souza, Ferraz, Albuquerque Araujo Seed rain of an abandoned agricultural area in a semiarid climate

5. remaining 94 plants arose from seed germination, and 54%
(51) of these produced seeds (yielding local seed rain). In the
mature forest, only 3.8% (5 of 129) of the selected individuals
originated from resprouting, and all of them produced fruit.
Of the 124 remaining plants originating from seed germina-
tion, 62.9% (78) produced fruit (Table S2).
Seed rain versus distance, season, habit and dispersal
syndrome
The species richness of the seed rain varied significantly with
distance (10–20 species per distance interval) (H = 132.44,
P 0.01), but no consistent pattern was observed (Fig. 3A).
Similarly, the number of diaspores varied from 300 to 1077
across the 21 distance intervals (H = 114.32, P 0.01) but did
not consistently increase or decrease with distance from the
mature forest (Fig. 3B). The distance from the mature forest
did not significantly influence the number of diaspores per
either habit or dispersal syndrome (F(1,239) = 1.23, P = 0.26;
Fig. 4). The number of diaspores per dry and rainy season and
per dispersal syndrome was not homogeneous among the dif-
ferent distance intervals in the young forest (Fig. 5). However,
there was a significant effect of the interaction between season
and dispersal syndrome on the number of diaspores
(F(2,239) = 15.74, P 0.01; Fig. 4), but this effect was only pres-
ent for self-dispersal, with a larger number of diaspores present
Fig. 2. Fruiting/dispersal periods for species in the mature and young forests and monthly seed rain in the young forest, Caruaru, Pernambuco, Brazil.
Plant Biology 16 (2014) 748–756 © 2013 German Botanical Society and The Royal Botanical Society of the Netherlands752
Seed rain of an abandoned agricultural area in a semiarid climate Souza, Ferraz, Albuquerque Araujo

6. during the dry season (mean Æ SE = 144.4 Æ 125) than in the
rainy season (48.3 Æ 60; Fig. 4).
The number of diaspores was also influenced by the interac-
tion between habit and dispersal syndrome (F(2,239) = 57.17,
P 0.001; Fig. 4). Diaspores from self-dispersing species pre-
dominated in the seed rain of woody species (153.6 Æ 120),
whereas diaspores dispersed by wind predominated in the seed
rain of herbaceous species (84.4 Æ 91; Fig. 4). However, the
number of diaspores dispersed by animals did not vary with
habit (Fig. 4), and diaspores dispersed in this way were rarely
found in the seed rain of the young forest. Only four species
exhibited dispersal by animals, three of which were dispersed
by seed hooks that attach to the exterior of the animals (Bidens
bipinnata, Bidens cf. pilosa and G. vaga; Table S1).
There was a significant reduction of allochthonous seed rain
with increasing distance from the mature forest (r2
= 0.66,
P 0.01). This seed rain was exclusively represented by M. uru-
ndeuva, S. brasiliensis, P. bahiensis and S. jacobinensis (Fig. 6).
DISCUSSION
Time of regeneration and recovery of species composition
The time elapsed since land use, the history of use, the respro-
uting ability of plants and the proximity to mature forest all
affect recolonisation of anthropogenic-disturbed areas (Pereira
et al. 2003; Levesque et al. 2011b; Lopes et al. 2012). Thus, con-
sidering the history of the young forest studied here (including
clear-cutting, planting and abandonment), the time since aban-
donment, the close proximity to a mature forest and the resil-
ience capacity of the community, we expected that the young
forest would have a species richness similar to that of the
mature forest and that the seed rain from woody species would
be predominantly local, with higher species richness and seed
quantity near the mature forest. However, of these expecta-
tions, there was only predominantly local seed rain, although it
was concentrated in a subset of the species.
Agricultural practices in humid and semiarid climates
impact plant diversity, pollinator guilds, seed dispersal and suc-
cession (Buisson et al. 2006; Almeida et al. 2011; Lopes et al.
2012). Consequently, recovery of species richness in abandoned
agricultural areas is slow, attaining 44% after 30 years of regen-
eration (Sampaio et al. 1998; Pereira et al. 2003). However, our
study showed that despite differing floristically from the
mature forest (i.e. sharing 50% similarity), the young forest
recovered approximately 34% (60/174 species) of its species
composition. This result demonstrates that maintaining pre-
served forests adjacent to agricultural areas may accelerate the
recovery rate of eliminated species.
However, as 79 species (29 woody and 50 herbaceous) from
the mature forest (Alcoforado-Filho et al. 2003; Araujo et al.
2005; Reis et al. 2006; Lucena et al. 2007; Oliveira et al. 2007)
were not observed in the young forest, and as 41 species from
the young forest (Lopes et al. 2012; Santos et al. 2013) were not
observed in the mature forest, some unidentified factors appear
to be inhibiting the recolonisation of species in this abandoned
agricultural area. Assuming the 41 species unique to the young
forest do not disappear during the succession process, these
results also suggest that the recolonisation of abandoned agri-
cultural areas may lead to forests that differ floristically from
those originally present. Most species absent from both forests
were autochorous, possibly reflecting the predominance of Mi-
mosaceae, Fabaceae, Caesalpiniaceae and Euphorbiaceae in the
caatinga vegetation, most of which have autochorous dispersal
(Lima et al. 2008; Souza 2010).
Influence of modes of regeneration on recolonisation of open
areas, and the importance of proximity to mature forests
In seasonally dry forests, the resprouting of plants is an impor-
tant strategy for the regeneration of anthropogenic-disturbed
A
B
Fig. 3. Variation in species richness (A) and diaspore density (B) of the seed
rain in the young forest of caatinga vegetation, Caruaru, Pernambuco, Brazil.
Fig. 4. Number of diaspores per habit (woody and herb), dispersal syn-
drome (self, wind and animal) and season (dry and rainy) in the young forest,
Caruaru, Pernambuco, Brazil. The same lowercase letters within and
between dispersal syndromes, habits and seasons indicate no significant dif-
ferences (P 0.05) according to analysis of covariance.
Plant Biology 16 (2014) 748–756 © 2013 German Botanical Society and The Royal Botanical Society of the Netherlands 753
Souza, Ferraz, Albuquerque Araujo Seed rain of an abandoned agricultural area in a semiarid climate

7. habitats because it accelerates the recolonisation of clear-cut
areas (Lugoa et al. 2004; Figueir^oa et al. 2006; Levesque et al.
2011b). This process is most efficient in areas with low pertur-
bation intensities (Kennard 2002). However, although we
found that 65% of the resprouting plants had fruits and, conse-
quently, contributed to the local seed rain, the number of
plants showing evidence of resprouting in the young forest was
low (22%), considering the history of use (only a single clear
cut). These results indicate that seed germination is a very
important strategy for establishing forest in agricultural areas.
Some species that originated from seed germination, such as
S. brasiliensis and B. cheilantha, are slow to reach reproductive
age, but others, including P. stipulacea, A. paniculata and
M. arenosa, flower and fruit within 18 years (Table S2). These
species are thought to be the initial colonisers during the suc-
cession of anthropogenic-disturbed areas of caatinga vegetation
(Pereira et al. 2003).
The relationship between seed rain density and distance
from the mature forest may or may not be significant (Holl
1998; Zimmerman et al. 2000; Cubi~na Aide 2001). In our
study, the three types of seed rain (autochthonous, allochtho-
nous and mixed) were detected in the young forest. After
18 years, the local and mixed seed rain made it difficult to eval-
uate the true effect of distance from the mature forest on the
seed rain of the young forest; however, neither the local or
mixed seed rain were considered in the analysis of distance
from mature forest.
Some studies of open pastures have found a reduction in
seed rain with increasing distance from forest, and demon-
strated that this relationship is strongly influenced by species
dispersed by wind (Zimmerman et al. 2000; Cubi~na Aide
2001). Our findings are consistent with this pattern, as the
main contributors to the allochthonous seed rain in the present
study (95% of diaspores) were species dispersed by wind,
most likely reflecting the absence of a closed canopy in the
young forest. Undoubtedly, some of the mixed seed rain was al-
Fig. 5. Annual and seasonal variation in seed rain dispersal syndromes (self-dispersal, wind dispersal and animal dispersal) in the young forest, Caruaru,
Pernambuco, Brazil.
Fig. 6. The relationship between allochthonous seed rain and distance from
the mature forest, Caruaru, Pernambuco, Brazil.
Plant Biology 16 (2014) 748–756 © 2013 German Botanical Society and The Royal Botanical Society of the Netherlands754
Seed rain of an abandoned agricultural area in a semiarid climate Souza, Ferraz, Albuquerque Araujo

8. lochthonous, and the absence of this component in the analysis
may have underestimated the contribution of the distance from
the mature forest to the allochthonous seed rain (Fig. 6). How-
ever, analysis of allochthonous seed rain alone showed that the
importance of proximity to mature forest is considerable and
contributes to the diversity and recovery of the young forest. For
example, there continue to be observable effects of the mature
forest on the recolonisation of several species, such as the endan-
gered M. urundeuva, a woody, dioecious, wind-dispersed species
that is very important economically for the local human com-
munities (Lucena et al. 2007; Oliveira et al. 2007).
In contrast, our analysis of local and mixed seed rain indi-
cates that the influence of nearby forest decreases with time
during the progress of succession, an observation made previ-
ously in other abandoned areas (Dungan et al. 2001; Kennard
2002; Letcher Chazdon 2009). Often, the progress of succes-
sion is evaluated through species composition, vegetation
structure and dispersal syndromes (Pereira et al. 2003; Jara-
Guerreiro et al. 2011; Martınez-Garza et al. 2011). However,
recent evidence from areas used for agriculture and grazing in
semiarid environments indicates that changes also occur in the
reproductive characteristics of plants, including flower produc-
tion and pollinator guilds (Almeida et al. 2011). Furthermore,
our study also recorded temporal displacement in the repro-
duction of some species (such as C. blanchetianus), which may
disappear as succession continues. Thus, we suggest that in
addition to species composition, vegetation structure and dis-
persal syndromes, the reproductive traits of plants may also be
used to evaluate forest recovery. However, more studies that
evaluate reproductive changes in additional species are needed
to verify these conclusions.
Factors limiting seed rain and implications for recolonisation
of agricultural areas
In semiarid climates, climate seasonality is one factor affect-
ing seed rain and the natural regeneration of forest. It does
so by influencing the amount of water available for plant
reproduction and by introducing temporal heterogeneity in
plant recruitment (Araujo et al. 2007; Levesque et al. 2011a,
b). In the present study, seasonality created temporal differ-
ences in the quantity of seeds in the seed rain. However,
although the seed rain from some species remained limited,
the overall seed quantity was high, indicating that the avail-
ability of seeds is no longer a limiting factor for recolonisa-
tion of the young forest. The seasonal changes we observed
in the seed rain of woody and herbaceous species (Table S1)
likely reflects that many of the herbaceous species are thero-
phytes; i.e. plants germinating, growing and producing seeds
in the rainy season and dispersing seeds and dying in the
dry season (Araujo et al. 2007). We also found that many
herbaceous individuals of species dispersed by wind or on
the surface of an animal, remained standing with their
diaspores after death. Their diaspores were liberated during
the dry season, as noted in Souza (2010).
Although proximity to mature forest promotes recolonisa-
tion of open areas (Young et al. 1987; Lopes et al. 2012), there
are situations in which proximity does not appear to affect
recolonisation. For example, Buisson et al. (2006) showed that
seed dispersal by wind and ants is limited in abandoned fields
in fragmented open grasslands, even when mature forests are
nearby. Others have reported that dispersal by animals reduced
seed rain from a mature forest because the animals do not
frequently venture into open, human-modified habitats (Holl
1998; Zimmerman et al. 2000; Cubi~na Aide 2001). In our
study, the low number of species represented in seed rain that
are dispersed by animals may reflect the open habitat of the
young forest.
Moreover, the predominant dispersal syndrome in dry
environments tends to vary with aridity and the predomi-
nance of life forms (herbs, vines, shrubs or trees). In some
dry forests, dispersal by animals predominates (Griz
Machado 2001; Jara-Guerreiro et al. 2011; Martınez-Garza
et al. 2011)’ however, in other forests (primarily in semiarid
environments), self-dispersal and wind dispersal predomi-
nate in both mature (Machado et al. 1997; Araujo et al.
2007; Lima et al. 2008) and anthropogenic-disturbed forests
(Teegalapalli et al. 2010), as reported in our study. Nonethe-
less, despite the predominance of autochorous species in
our study, species dispersed by animals were least repre-
sented in the young forest, indicating that dispersal by ani-
mals has not yet been completely re-established. Some self-
dispersed species are also dispersed secondarily by ants (Leal
et al. 2007; Lobo et al. 2011). Our study did not measure
secondary dispersal, but it is possible that dispersal by ants
has been limited, as in other human-disturbed areas (Buis-
son et al. 2006). This issue warrants further study.
In summary, proximity to mature forest favours seed rain
into young forest. Although seed availability does not appear
to be a limiting factor for recolonisation, the species richness of
the young forest has not fully recovered even after 18 years,
and our results suggest that it may also differ floristically from
the mature forest in the future. Some species may require a
temporal shift in their reproductive period before the forest
becomes mature again. As seed germination is particularly
important for the recolonisation of previously cultivated areas,
the factors that negatively affect seed rain, seed survival in the
soil seed bank and the germination process itself must be better
understood to predict the restoration potential of dry forests in
abandoned agricultural areas.
ACKNOWLEDGEMENTS
We thank Everardo Sampaio, Marcelo Tabarelli and Luiz Maran-
gon for their contributions to the manuscript, and the Conselho
Nacional de Desenvolvimento Cientıfico e Tecnologico for finan-
cial support (Grants: 471805/2007-6, 301720/2010-0, 508822/
2010-6 and 4772392009-9) and the scholarships provided. We
also thank the Instituto Agron^omico de Pernambuco (IPA) for
logistic support, and the taxonomists Olivia Cano, Rita Pereira,
Ana Du’Bocage, Maria Bernadete and Jorge Irapu~a.
SUPPORTING INFORMATION
Additional Supporting Information may be found in the online
version of this article:
Table S1. Number of diaspores per species per month in the
5.48 m2 sampled area in the young caatinga forest, Caruaru,
Pernambuco, Brazil.
Table S2. Fruiting and evidence of regrowth of plants from
populations in the young and mature forests in Caruaru, Per-
nambuco, Brazil.
Plant Biology 16 (2014) 748–756 © 2013 German Botanical Society and The Royal Botanical Society of the Netherlands 755
Souza, Ferraz, Albuquerque Araujo Seed rain of an abandoned agricultural area in a semiarid climate

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Seed rain of an abandoned agricultural area in a semiarid climate Souza, Ferraz, Albuquerque Araujo