Spatial distribution of seeds and juveniles of Enterolobium glaziovii Bentham (Leguminosae, Mimosoideae) in the Atlantic forest, Brazil

Abstract

The spatial distribution of fruits and juveniles of Enterolobium glaziovii Bentham were evaluated in four circular plots of 30 m radius, centered around reproductive individuals to determine whether the size of the parental crowns, topography, and canopy coverage influence these patterns. Each crown was subdivided into eight irregular triangles and the area of each was calculated. Each plot was subdivided into four sub-plots, two of them in an up-slope direction, and the other two in a down-slope direction. The canopy coverage for each plot was estimated at breast height (1.30 m) and at ground level, every three months during 1998. The numbers of fruits and juveniles of E. glaziovii were recorded. Although there were more fruit under the parental crown (F1,12 = 0.01; p = 0.92), there was no difference in the number of juveniles under and beyond the reproductive trees (F1,12 = 0.88; p = 0.36). There was a positive correlation between the areas of the crowns and the numbers of fruits and juveniles under them (r = 0.62; df = 14; p < 0.05). Most of the fruits and juveniles were found in the down-slope directions. The canopy coverage was lower in spring, but higher under parental crowns (only at breast height). These results indicate that the parental crown, topography and canopy coverage influenced the pattern of spatial distribution and probably also the dynamics of E. glaziovii seeds and juveniles.

Full text

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Acta bot. bras. 19(3): 609-614. 2005
Spatial distribution of seeds and juveniles of Enterolobium glaziovii
Bentham (Leguminosae, Mimosoideae) in the Atlantic forest, Brazil
Flavio Nunes Ramos1,3, Dalva M. Silva Matos2 and Flavio A.M. Santos1
Received: July 23, 2004. Accepted: February 16, 2005
RESUMO – (Distribuição espacial de sementes e juvenis de Enterolobium glaziovii (Leguminosae, Mimosoidade) na mata Atlântica,
Brasil). Os padrões de distribuição espacial de frutos e juvenis de Enterobium glaziovii Bentham foram avaliados em quatro parcelas
circulares de 30 m de raio, centralizadas em uma árvore reprodutiva para determinar se o tamanho das copas das plantas parentais,
topografia e cobertura de dossel influenciam esses padrões. Cada copa foi subdividida em oito triângulos irregulares e suas áreas
calculadas. Cada parcela foi subdividida em quatro sub-parcelas, sendo duas nos terrenos inclinados para cima e duas nos inclinados para
baixo. A cobertura de dossel de cada parcela foi estimada tanto na altura do peito (1,30 m), quanto na altura do chão, a cada três meses em
1998. O número de frutos e juvenis de E. glaziovii foi quantificado. Apesar de ter havido mais frutos debaixo da copa da arvore parental
(F1,12 = 0.01; p = 0,92), não houve diferenças no número de juvenis embaixo ou fora da copa da planta parental (F1,12 = 0,88; p = 0,36).
Houve correlação positiva entre a área das copas e o número de frutos e juvenis embaixo delas (r = 0,62; df = 14; p < 0,05). A maioria dos
frutos e juvenis foi encontrada nos terrenos inclinados para baixo. A cobertura de dossel foi menor na primavera, porém maior embaixo
da copa das plantas reprodutivas (apenas na altura do peito). Esses resultados indicam que a copa das plantas parentais, topografia e
cobertura de dossel influenciam o padrão de distribuição espacial e provavelmente também a dinâmica de sementes e juvenis de
E. glaziovii.
Palavras-chave: chuva de sementes, influência do parental, tamanho da copa, topografia
ABSTRACT – (Spatial distribution of seeds and juveniles of Enterolobium glaziovii Bentham (Leguminosae, Mimosoideae) in the
Atlantic forest, Brazil). The spatial distribution of fruits and juveniles of Enterolobium glaziovii Bentham were evaluated in four circular
plots of 30 m radius, centered around reproductive individuals to determine whether the size of the parental crowns, topography, and
canopy coverage influence these patterns. Each crown was subdivided into eight irregular triangles and the area of each was calculated.
Each plot was subdivided into four sub-plots, two of them in an up-slope direction, and the other two in a down-slope direction. The
canopy coverage for each plot was estimated at breast height (1.30 m) and at ground level, every three months during 1998. The numbers
of fruits and juveniles of E. glaziovii were recorded. Although there were more fruit under the parental crown (F1,12 = 0.01; p = 0.92),
there was no difference in the number of juveniles under and beyond the reproductive trees (F1,12 = 0.88; p = 0.36). There was a positive
correlation between the areas of the crowns and the numbers of fruits and juveniles under them (r = 0.62; df = 14; p < 0.05). Most of the
fruits and juveniles were found in the down-slope directions. The canopy coverage was lower in spring, but higher under parental crowns
(only at breast height). These results indicate that the parental crown, topography and canopy coverage influenced the pattern of spatial
distribution and probably also the dynamics of E. glaziovii seeds and juveniles.
Key words: conspecific influence, crown size, seed shadow, topography
1Universidade de Campinas, Instituto de Biologia, Departamento de Botânica, C. Postal 6109, CEP 13083-970, Campinas, SP, Brazil
2Departamento de Ciências Naturais, UNIRIO, Av. Pasteur 458, Urca, CEP 22290-240, Rio de Janeiro, RJ, Brazil
3Corresponding Author: fnramos@gmail.com
Introduction
The potential spatial distribution of plants within a
population is determined by the distribution of seeds
during dispersal (Clark & Clark 1984). Seed dispersal
is the last step in the reproductive cycle of plants, but
also the starting point in the process of population
renewal and recruitment (Herrera et al. 1994). The
seed shadow of a tree species is a function of the
efficiency of the dispersal agents, and of the tree’s
productivity (Janzen 1970), as well as soil conditions
and microtopography (Loiselle et al. 1996). The post
dispersal seed distribution is important because the
growth and survival of plants depends on the locations
reached by the seeds (Schupp 1988).
The probability of fruit or seeds falling far from
the parent plants is dependent on their size or mass.
Usually, a very large fraction of the total seeds fall

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close to the parental tree (Howe et al. 1985; Forget
1989), and the fraction is greatest for heavy seeds
dispersed by gravity (Richards 1996). Seed dispersal
by gravity or barochory is often characteristic of huge
fruits with no other morphological features that enable
them to be dispersed primarily by biotic (e.g., bats, birds,
monkeys, elephants, rodents) or abiotic (e.g., wind,
water) agents (Forget 1992b). According to Denslow
(1980), the sizes and shapes of seed and perhaps
seedling shadows of species that bear heavy fruit are
expected to be related to the area of the parental crown
and to topography. The spatial distribution of light is
another important factor that may determine the
seedling shadow (Smith et al. 1992).
The aim of this study was to describe the spatial
distribution of E. glaziovii fruits and juveniles in order
to answer the following questions: Do the sizes of
parental crowns influence the spatial distributions of
fruits and juveniles? Does topography influence the
spatial distribution of fruit and juveniles of E. glaziovii?
Does canopy coverage influence the spatial distribution
of its juveniles?
Material and methods
Study area – The study was carried out in Biological
Reserve of Poço das Antas (BIORE) (22°29’ -
22°36’S, 42°13’ - 42°21’W) and in the Parque
Nacional da Tijuca, near the Rio de Janeiro Botanical
Garden (RJBG) (22°58’S, 43°13’W) in Rio de Janeiro
State, Brazil. Four circular plots with 30 m of radius
each centered (2827.35 m2 each plot) around a
reproductive tree of Enterolobium glaziovii
Bentahm. Three of the plots (B1, B2 and B3) were
in BIORE and one of them (R1) was in RJBG. Both
areas are classified as evergreen forest, or
Ombrophilous Dense Forest (Velloso et al. 1991).
The mean annual temperature at the BIORE is
27.6 °C in the summer and 21.3 °C in the winter, with
a mean annual rainfall of 2,092 mm (IBDF 1981b
and data from the Golden Lion Tamarin Association
collected from 1983 to 1998). In the RJBG, the mean
annual temperature is 29 °C in the summer and 22 °C
in the winter, with a mean annual rainfall of 1,075 mm
(IBDF 1981a; Oliveira & Lacerda 1988). All of the
reproductive trees studied were isolated and very far
from each other (no other E. glaziovii were found in
these areas). BIORE and RJBG plots were separated
by 126 km and the BIORE trees were 2.5-10 km
apart. All of the plots were on slopes, where the
inclination raged to 1.3° from 60° (Ramos 200).
Study species – Enterolobium (Leguminosae -
Mimosoideae) is a neotropical genus distributed from
Central America (Mexico) to South America
(Argentina), with the Amazon being the center of
diversity (Mesquita 1990). The timber of this genus is
used to make boats and packing cases. Enterolobium
species are distinguished mainly by their fruit
morphology, which is predominantly indehiscent.
Among the 10 species of the genus, E. glaziovii has a
restricted geographic distribution and is only found in
three states in Brazil: Rio de Janeiro, Espirito Santo
(SE Brazil) and Bahia (NE Brazil), being endemic to
the Brazilian Coastal Atlantic forests (Mesquita 1990).
This species, which occurs at a low frequency in forest
sites (Lima, H.C. Botanical Garden of Rio de Janeiro,
Brazil, pers. comm.), is a deciduous canopy tree with
reproductive individuals ranging from 8-30 m in height
(Mesquita 1990). Fruiting occurs in May and June and
the tree loses its leaves in May, June and July. The
contorted black woody fruits are large
(8-10 cm×4-5 cm) and heavy (14.6±6.4 g) (Mesquita
1990) and contain 1-14 seeds, (mean of 9 seeds) (F.N.
Ramos & A.C.S. Andrade, data not published). No
predation on seeds inside fallen fruits was observed in
this study (F.N. Ramos & A.C.S. Andrade, data not
published).
Distribution of fruit and juveniles – The number of
E. glaziovii juveniles was monitored in the circular
plots from 1996 to 1999, and the number of fruit in
each circular plot was sampled using four 30 m long
wedges of 5°, extending in each of the four cardinal
compass directions away from the central reproductive
tree. The distance of all fruits from the parental tree
was recorded in 1998 and 1999, as soon as the fruit
fell. All E. glaziovii juveniles were marked.
Crown size – To assess the influence of the size and
asymmetry of parental crowns on the spatial distribution
of fruit and juveniles, each crown was divided into eight
irregular triangles and the area (m2) of each triangle
was calculated by trigonometric relations. The distance
from the bole to the crown edges of the individual was
measured constructing a system of four wedges of 90°
in each of the four cardinal compass directions. The
crown asymmetry was obtained by dividing the crown
in halves, considering the maximum value among the
possible pairs. The maximum value was calculated by
dividing the largest of these two halves by the total
area (Amax / Atotal). This value varied between 0.5
(symmetry) and 1.0 (“complete” asymmetry) (Young
& Perkocha 1994). The number of fruits and juveniles

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Acta bot. bras. 19(3): 609-614. 2005.
611
of E. glaziovii was determined under and beyond the
crown and under each of the four crown triangles.
Topography – To assess the influence of topography
on the spatial distribution of the fruits and juveniles of
E. glaziovii, each plot, which was on a slope, was
partitioned into two sub-plots in an up-slope direction
(areas above the individual) and two sub-plots in a
down-slope direction (areas below individual). The
number of fruits and juveniles of E. glaziovii in each
sub-plot was recorded.
Canopy coverage – Canopy coverage values were
estimated at 1.30 m (breast height) and at ground
height using a spherical concave densiometer. Samples
were taken every 5 m, from the central E. glaziovii to
the boundary of each plot, along eight transects in the
compass directions. The canopy coverage values were
estimated every three months (at the beginning of each
season) during 1998. Thus, for each season, canopy
coverage values were recorded from 48 points at each
height in each plot.
Statistical analysis – All data expressed as proportions
were arcsine transformed before analysis to improve
the homocedasticity and normality of the distributions,
and were back-transformed in the tables and figures
(Zar 1996). Differences in the proportions of fruits and
juveniles of E. glaziovii between under and beyond
the parental tree crowns and among years, and also
between up and down - slope sites and among years
were tested by two-way ANOVA. The canopy
coverage between under and beyond the parental tree
crowns and among seasons, and between up and down
- slope and among seasons, were also compared by
two-way ANOVA.
The Pearson correlation coefficient was used to
examine the relationship between the area of each
parental crown triangle and the mean proportion of
fruit (among years) and also between the area of each
parental crown triangles and the mean proportion of
juveniles (among years) under it. This correlation
coefficient was also used to assess the relationship
between the median distance of the fruit from the
parental tree and the size of the radii of the parental
crown. The crown triangle areas were square root
transformated before the correlation test.
Results
Crown size – The crown radii of the trees ranged from
5.1 m to 12.4 m and the crown areas ranged from
163.1 to 541.2 m2. All trees had asymmetric crowns
(0.67 to 0.94) that were offset in the down-slope
direction. The crown triangles that had greater areas
also had a greater number of fruit (r = 0.62; df = 14;
p < 0.05) and juveniles (r = 0.51; df = 14; p < 0.05)
under them. However, there was no correlation
between the radii of the parental crowns and the median
distance of fruit from the parental bole (r = 0.40; df = 6;
p > 0.05) in sub-plots in the down-slope direction. In
other words, greater crown radii did not represent an
increase in the median distance of the fruit, from the
bole to down-slope directions.
Distribution of fruit and juveniles – Seeds were only
found inside the fruit. Although there were more fruit
(F1,12 = 52.5; p = 0.001) under the parental crown than
beyond (Fig. 1) in both years (F1,12 = 0.01; p = 0.92),
there were no significant differences in the numbers
of juveniles under and beyond the crowns (F1,12 = 0.88;
p = 0.36) or among the years (F3,12 = 0.01; p = 0.99)
(Fig. 2). However, there were significantly more fruits
(F1,12 = 26.2; p = 0.001) (Fig. 1) and more juveniles
(F1,12 = 49.3; p = 0.001) in the down-slope direction
than up-slope (Fig. 2), in both years (F1,12 = 0.01;
p = 0.92 and F3,12 = 0.01; p = 0.99, respectively).
Canopy coverage – The canopy coverage at the two
heights was different. There was greater canopy
coverage (CC) at 1.30 m under the parental crowns
than beyond it (F1,12 = 37.2; p = 0.001) and in the up-
slope direction compared to the down-slope
(F1,12 = 6.6; p = 0.011). Additionally, CC was lower in
Spring, than the other seasons (F1,12 = 3.4; p = 0.019
and F1,12 = 3.2; p = 0.024, respectively) (Fig. 3). In
contrast, there were no significant differences in CC
at ground height under or beyond the parental crowns
Fruit percentage (%)
Under Beyond Down-slopeUp-slope
Figure 1. Percentage (mean ± SD) of fruit of Enterolobium glaziovii
Bentham under and beyond the central reproductive tree crown
and in up- and down-slope directions in 1998 and 1999. The data
were back transformed from the arcsine values. There were more
fruit (F1,12 = 52.5; p = 0.001) under the parental crown than
beyond and in the down-slope direction than up-slope (F1,12 =
26.2; p = 0.001) in both years. ? = 1998; ? = 1999.
125
0
25
50
75
100
a A b B a A b B

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(F1,12 = 0.29; p = 0.59) or in the up- or down-slope
direction (F1,12 = 0.26; p = 0.61), although CC was
lower in Spring than the other seasons (F1,12 = 6.5;
p = 0.001 and F3,12 = 6.8; p = 0.001, respectively)
(Fig. 4). All of the E. glaziovii juveniles were found
under a canopy coverage of > 80%, with most of them
under a CC > 90% (Tab. 1), however most of the CC
values (82.4%) were above 80%.
Juvenile percentage (%)
Under BeyondDown-slopeUp-slope
Figure 2. Percentage (mean ± SD) of juveniles of Enterolobium
glaziovii Bentham under and beyond the central reproductive
trees crowns and in up- and down-slope directions from 1996 to
1999. The data were back transformed from the arcsine values.
There were no significant differences in the numbers of juveniles
under and beyond the crowns (F1,12 = 0.88; p = 0.36), but there
were significantly more juveniles (F1,12 = 49.3; p = 0.001) in the
down-slope direction than up-slope in all years. ? = 1996;
? = 1997; ? = 1998; ? = 1999.
Figure 4. Percentage (mean ± SE) of canopy coverage (CC) of
Enterolobium glaziovii Bentham at ground height under and
beyond the central reproductive trees crowns and in up- and
down-slope directions in each season. The data were back
transformed from the arcsine values. The only differences is that
CC was lower in Spring than the other seasons (F1,12 = 6.5;
p = 0.001. ? = Spring; ? = Summer; ? = Autumn; ? = Winter.
Canopy coverage (%)
UnderBeyond Down-slopeUp-slope
Figure 3. Percentage (mean ± SE) of canopy coverage (CC, %) of
Enterolobium glaziovii Bentham at breast height under and beyond
the central reproductive trees crowns and in up- and down-slope
directions in each season. The data were back transformed from
the arcsine values. There was greater canopy coverage under the
parental crowns than beyond it (F1,12 = 37.2; p = 0.001) and in the
up-slope direction compared to the down-slope (F1,12 = 6.6; p =
0.011). CC was lower in Spring, than the other seasons (F1,12 = 3.4;
p = 0.019). ? = Spring; ? = Summer; ? = Autumn; ? = Winter.
Discussion
Juveniles of barochoric species generally grow
near the parental trees, in a low light intensity
environment (Forget 1992a). Studies of seed rain and
seedling survivorship have shown that early seedling
Table 1. Percentage of Enterolobium glaziovii Bentham offspring
and the percentage of canopy coverage (CC) values measured
sampled on each canopy coverage class (%) in 1998.
CC classesCC measuredOffspring (%)
100-90
80-90
0-80
48.2
34.2
17.6
82.4
17.6
0.0
recruitment may be spatially correlated with the seed
rain, although this relationship may disappear as the
seedlings age and become saplings (Herrera et al.
1994). High canopy coverage values (>80%) could limit
the range of plant species that are able to germinate,
establish and growth around E. glaziovii adults.The
results show the recently dispersed seeds of
E. glaziovii, which its germination are not influenced
by light (Ramos & Santos, unpubl. data), are not
exposed to light, because up to 1.3 m of height there
was no difference in CC between under and beyond
the central reproductive tree crown and between up-
and down-slope directions. E. glaziovii seeds are
dispersed on the ground and germinated differently in
time due to its differential dormancy. It seems the
seedlings recruit and grow without much light influence
until they achieve about 1.30 m of height, when the
light begins influenced it. The juveniles beyond the
central reproductive tree crown and in down-slope
directions are under greater luminosity e consequently
have greater chances of growth and establishment.
Canopy coverage (%)
UnderBeyondDown-slopeUp-slope

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Acta bot. bras. 19(3): 609-614. 2005.
613
Ramos & Santos (unpubl. data) show the juveniles
greater than 50 cm of height grew more than the smaller
ones. Additionally, in the spring or in the dry season,
when the deciduous trees lost its leaves and
consequently the light in the understory increase, may
be the time when E. glaziovii juveniles have most of
their height increment. However, in order to verify it, a
study of the growth of each E. glaziovii juvenile during
each season of the year would be necessary.
There was spatial and temporal variation in canopy
coverage (CC). CC was lower in the Spring than in
the other seasons, and there were differences between
CC at breast height and at ground height. Although
CC at ground height was homogeneous in the plots,
CC at breast height was greater under the parental
crown and in the up-slope direction. Most of the CC
values were high (>80%), since there were few small
gaps in the plots. The difference between CC at breast
height and at ground height also indicated that the light
intensity reaching small plants and early seedlings was
less than that reaching saplings or shrubs ≥ 1.5 m tall.
The availability of light is probably a very important
factor in the spatial distribution of juveniles, influencing
their survival chances. The seasonal deciduousness of
E. glaziovii adults generated fluctuations in the CC of
the plots. E. glaziovii was probably, and the most
important deciduous tree species in the plots since its
crown covered about 1/3 of each plot area.
Clumps of fruit under parental plants, such as
observed here for E. glaziovii, have been found for
many other plant species, especially those with heavy
fruit (Forget 1989; 1992b; Herrera et al. 1994; Negi
et al. 1996), such as Eperua grandiflora (Aublet)
Benth. in French Guiana, in which most of the fruit
occurs under the parental crown (Forget 1992a).
Laman (1996) found that more than 50% of the fruits
of two Ficus species (which bear small fruit), in a
Bornean rain forest, fell under their own crown. The
shape and size of the adult crown may influence the
seed distribution on the ground (Ramirez & Arroyo
1987). E. glaziovii trees with greater crown areas had
more fruits and juveniles under them, in contrast to
Copaifera publiflora Benth., for which trees with a
smaller crown area presented greater seed density at
the crown edge while trees with a larger crown area
had greater seed density near the trunk (Ramirez &
Arroyo 1987).
The slope of the ground presents a strong influence
on the fruit and seed shadow of barochoric species
because fruit that falls to the ground can roll down the
slope (Forget 1992a). Rain and trampling by animals
can also contribute to the fruit being spread down-slope.
The distribution of fruit and juveniles of E. glaziovii in
the down-slope direction was similar to that found in a
Bombacaceae species in Colombia (Denslow 1980),
and Eperua grandiflora in French Guiana (Forget
1992a), both of which have large fruit. All of the plots
studied were on slopes, although there was
considerable variation in their declivities (F.N. Ramos,
data not publushed). Since most of the fruits and
juveniles occurred in the down-slope direction, there
must be factors that help maintain this species in a
sloping area and prevent it from descending to a flat
region. According to Forget (1992a), secondary
dispersers may help to distribute the fruit and seeds
more homogeneously in the down- and up-slope
directions. Secondary seed dispersal on the upper side
of the slope could lead to gradual ridge colonization,
and compensate for the slope effect that drives most
of the seeds down the slope (Forget 1992b). However,
the seed shadow in the plots studied probably has been
little influenced by frugivorous animals in the last years,
since there was abundant fruit on the ground that had
not been touched for more than a year, in all of the
plots. This could reflect the hunting activity of humans
in the two reserves where the plots were located
(Hydson Pinheiro, IBAMA, pers. com.), since hunting
would reduce the number of fruit consumers. So, the
future of this species could be threatened.
In conclusion, variation in crown size, topography
and CC (spatial and temporal) together, seem to
influence the distribution of E. glaziovii fruits and
juveniles, creating an initial spatial distribution from fruits
and influence a different distribution of juveniles. For
example, seeds that fall far from parental trees have a
greater chance of surviving (Ramos et al., unpubl.
data). Therefore, the biotic and abiotic characteristics
identified in this study may have contributed to our
understanding of the dynamics of tree seedlings and
juveniles.
Acknowledgements
The author thanks to Alexandre Fadigas de Souzas,
Mariana Cassab Torres, Jose Filipe Caluca, Ludimila
Siqueira, Rita Portela, Maria Isabel Braz, Leonardo
Lima, Tiago Bosisio Quental, Jorge Nascimento, Jair
Lage Siqueira Neto and Antônio Maximo Rosa for help
in the field work, and the Golden Lion Tamarin
Association for data on rainfall and temperature in the
Biological Reserve of Poço das Antas. Alexandre
Adalardo Oliveira, Fernando Roberto Martins, Gislene

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614
Maria Ganade and Marcelo Teixeira Nascimento
provided stimulating comments on the manuscript. This
work was supported by Fundação de Amparo à
Pesquisa do Estado de São Paulo (FAPESP) - Grant
nº 98/01264-0.
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