Forest Ecology and Management 256 (2008) 1910–1917

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Forest Ecology and Management

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Profound impoverishment of the large-tree stand in a hyper-fragmented

landscape of the Atlantic forest
M.A. Oliveira, A.M.M. Santos, M. Tabarelli *
Departamento de Botânica, Universidade Federal de Pernambuco, 50670-901 Recife, PE, Brazil

A R T I C L E I N F O A B S T R A C T

Article history: Large tree species have a disproportional influence on the structure and functioning of tropical forests,
Received 22 January 2008 but the forces affecting their long-term persistence in human-dominated landscapes remain poorly
Received in revised form 3 July 2008 understood. Here we test the hypothesis that aging forest edges and small fragments (3.4–295.7 ha) are
Accepted 17 July 2008
greatly impoverished in terms of species richness and abundance of large trees in comparison to core
areas of forest interior. The study was conducted in a hyper-fragmented landscape of the Atlantic forest,
Keywords:
northeast Brazil. Large tree species were quantified by recording all trees (DBH  10 cm) within fifty-
Anthropogenic landscapes
eight 0.1-ha plots distributed in three forest habitats: small forest fragments (n = 28), forest edges
Edge effects
Forest emergent layer
(n = 10), and primary forest interior areas within an exceptional large forest remnant (n = 20). Large tree
Habitat fragmentation species and their stems 10 cm DBH were reduced by half in forest edges and fragments. Moreover, these
Large trees edge-affected habitats almost lacked large-stemmed trees altogether (0.24  0.27% of all stems sampled),
and very tall trees were completely absent from forest edges. In contrast, large trees contributed to over 1.5%
of the whole stand in forest interior plots (2.9  2.8%). Habitats also differed in terms of tree architecture:
relative to their DBH trees were on average 30% shorter in small fragments and forest edges. Finally, an
indicator species analysis yielded an ecological group of 12 large tree species that were significantly
associated with forest interior plots, but were completely missing from edge-affected habitats. Our results
suggest a persistent and substantial impoverishment of the large-tree stand, including the structural collapse
of forest emergent layer, in aging, hyper-fragmented landscapes.
ß 2008 Elsevier B.V. All rights reserved.

1. Introduction be permanently favored in truly hyper-fragmented landscapes

Collectively, habitat loss and fragmentation represent the most
pervasive and disturbing results of present-day human land use
dynamics (Wright, 2005; Laurance et al., 2007). As human
population continues to expand, even vast remote tracts of old-
growth tropical forests are likely to be converted into severely
fragmented landscapes (Aide and Grau, 2004; Wright and Muller-
Landau, 2006) and force small fragments to remain embedded
within open-habitat matrices (Turner and Corlett, 1996; Gascon
et al., 2000). Increasing empirical evidence indicates that habitat
fragmentation rapidly drives many ecological groups of tree
species to decline at landscape scale, such as large-seeded trees
that are gut dispersed by vertebrates (Stoner et al., 2007),
desiccation-sensitive shade-tolerant species (Laurance, 2001),
and tree species depending on long-distance pollen movement
and animal-mediated pollination services (Laurance et al., 2006;
Girão et al., 2007). In contrast, some short-lived pioneers appear to
* Corresponding author. Tel.: +55 81 2126 8945; fax: +55 81 2126 8348.
E-mail address: mtrelli@ufpe.br (M. Tabarelli).
(Tabarelli et al., 1999; Oliveira et al., 2004; Michalski et al., 2007).
These shifts in the functional profile of tree assemblages, including
the collapse of aboveground biomass, have been recently described
as a fragmentation-induced degeneration process (Santos et al.,
2008), which may impair conservation and ecosystem services, as
well as the economic opportunities provided by forest remnants
embedded in anthropogenic landscapes (see Nascimento and
Laurance, 2004; Michalski et al., 2007).
Large-stemmed (DBH > 70 cm) and very tall trees (>31 m
height) represent the most conspicuous population component of
the canopy/emergent tree species, and their large crowns
constitute one of the building blocks of tropical forests—the
emergent layer (Primack and Corlett, 2005). In the lowland forests,
large canopy and emergent tree species (hereafter referred to as
large tree species) usually represent less than 10% of the overall
tree species richness (10 cm DBH), and their large individuals
account for 1–6% of all tree stems (Clark and Clark, 1992; Oliveira
and Mori, 1999; Turner, 2001; Small et al., 2004; Castilho et al.,
2006). However, large trees provide a disproportional contribution
regarding aboveground biomass, nutrient cycling and carbon
storage (Chambers et al., 2001; Nascimento and Laurance, 2004;

0378-1127/$ – see front matter ß 2008 Elsevier B.V. All rights reserved.
doi:10.1016/j.foreco.2008.07.014
 M.A. Oliveira et al. / Forest Ecology and Management 256 (2008) 1910–1917
Vieira et al., 2004), primary productivity (Chambers et al., 1998),
and the natural disturbance regime driven by treefall gaps
(Brokaw, 1982; Putz, 1983). Although the full complement of
organisms inhabiting the emergent layer is yet to be documented
(see Lowman and Nadkarni, 1995), it is likely that a substantial
portion of tropical forest biodiversity relies on resources provided
by the sun-exposed crowns of large trees as they provide an
irreplaceable light environment. Through mast events of repro-
duction, for example, several emergent tree species can tempora-
rily offer to herbivores immense supplies of flower, fruit and seed
resources (Gribel et al., 1999; Curran and Leighton, 2000; Newbery
et al., 2006). Many birds and primates, in fact, are strictly
dependent on large trees for nesting or food supply, leading
several large tree species to be recognized as key-stone plants (see
Poonswad, 1995; Peres, 2000; Delannoy and Tossas, 2002).
Unfortunately, large trees appear to be highly vulnerable to
habitat fragmentation and the establishment of artificial forest
edges. Long-term tree inventories in the Amazon region have
documented a chronic, increased mortality of large trees near forest
edges surrounded by open habitats (Laurance et al., 2000;
Nascimento and Laurance, 2004). Specifically, large trees may face
a 40% increase in mortality near edges (particularly in the aftermath
of habitat fragmentation) and die three times faster than those
inhabiting spots located over 300 m into the forest (Laurance et al.,
2000) due to elevated rates of uprooting and breakage caused by
increased wind turbulence near forest edges: the ‘‘wind damage
hypothesis’’ (sensu D’Angelo et al., 2004). In addition to this direct,
edge-induced mortality, surface forest fires and logging may
constitute aggravating sources of large tree mortality in human-
impacted, fragmented landscapes (Barlow et al., 2003). However,
increased mortality has been documented primarily in recently
created fragmented landscapes, severely limiting accurate insights
about the long-term persistence of large trees in consolidated,
human-dominated landscapes. Assuming that the edge-induced
mortality observed in the Amazon region represents a more
persistent fragmentation-related effect, one would expect a
profound impoverishment or even the structural collapse of the
large-tree stand in aging, hyper-fragmented landscapes, regardless
of whether these landscapes have experienced expressive forest
fires and logging. This prediction has not been examined thoroughly
despite its far-reaching consequences for biodiversity conservation
in landscapes vastly dominated by edge-affected habitats.
Therefore in this study we examine whether edge-affected
habitats are able to retain the large-tree stand and the forest
emergent layer in a hyper-fragmented landscape of the Atlantic
forest with no detectable signs of forest fires and logging. In
particular, we test the hypothesis that aging forest edges and small
fragments (3.4–295.7 ha) are greatly impoverished in terms of
species richness and abundance of large trees in comparison to
forest interior patches of an exceptionally large fragment (the
control area). First, we provide scores for the relative importance of
large tree species and their stems 10 cm DBH within these three
habitats—forest edges, small fragments and primary forest interior
areas. Second, we describe tree distribution within categories of
DBH and height, and tree architecture across the habitats. Third, a
set of large tree species serving as indicator species of the forest
interior habitat is presented. Finally, we address plausible edge-
related mechanisms driving the impoverishment of the large-tree
stand and its potential implications for the persistence of
biodiversity in anthropogenic, hyper-fragmented landscapes.
2. Study area
This study took place at Usina Serra Grande, a private sugar-
cane landholding located in the State of Alagoas, northeastern
1911
Brazil (88300 S, 358500 W). We selected an aging, large (667 km2)
hyper-fragmented landscape containing 109 forest fragments, all
of which are entirely surrounded by a uniform, stable and
inhospitable matrix of sugar-cane monoculture (Fig. 1). Sugar-
cane cultivation in this landscape dates back at least to the 19th
century, and the remaining forest has been protected against
wildfires and logging to provide watershed protection and water
supply for sugar-cane irrigation (Santos et al., 2008). This has
ensured the positional stability of forest fragment borders and the
subsequent establishment of reproductive pioneer and shade-
tolerant trees along post-closure forest edges (Melo et al., 2006).
Currently, 9.2% of forest cover is left, including the 3500-ha
Coimbra Forest—the largest and best preserved forest patch in the
region (Grillo et al., 2006). Coimbra still retains a full complement
of plant and vertebrate groups typical of vast undisturbed tracts of
Atlantic forest, including large-seeded trees, large frugivorous
birds, and large populations of valuable timber trees such as the
softwood Ucuuba (Virola gardneri) and the hardwoods Sapucaia
(Lecythis pisonis) and Jatoba (Hymenaea courbaril); see Pôrto et al.
(2006) for a comprehensive mutitaxa checklist of plant and
vertebrate species inhabiting the Serra Grande landscape. The
predominantly lowland terra firme forest (sensu Whitmore, 1998)
includes two physiognomic subtypes: evergreen and semi-
deciduous forests (Veloso et al., 1991). Leguminosae, Lauraceae,
Sapotaceae, Moraceae, Chrysobalanaceae and Euphorbiaceae
account for half of tree species richness (Grillo et al., 2006).
3. Methods
3.1. Tree surveys and large tree species
In 2003–2004, all live trees 10 cm in diameter at breast height
(DBH) were inventoried within fifty-eight georeferenced 0.1-ha
plots (10 m  100 m) in three habitats (as described in Santos et al.,
2008)—(1) forest edge: 10 plots located in the peripheral areas
within 100 m of the border of the largest fragment (the Coimbra
Forest, 3500 ha); (2) core area: 20 plots located in the old-growth
forest interior of Coimbra Forest beyond 200 m of any border and
showing no detectable edge influence; (3) small forest fragments:
one plot per fragment located at the geometric center of 28 forest
fragments ranging between 3.4 and 295.7 ha in size and being
entirely surrounded by sugar-cane fields. The distance between
plots and the nearest forest edge was 0 m for edge plots, 200–
1012.7 m for forest interior plots, and 60.4–502.7 m for plots in
forest fragments. The average distance between all 58 plots
exceeded 1000 m. All trees 10 cm DBH within the 58 plots had
their diameter at breast height measured and total height visually
estimated (upper crown height). Height estimates were provided
exclusively by Oliveira, who initially calibrated his estimates
against previously height-measured poles. In order to reduce the
influence of any error in these estimates, tree heights were
assigned within seven broad classes of height. Trees were
identified to species level and plant vouchers are available at
the Federal University of Pernambuco (UFP) Herbarium, Brazil
(voucher nos. 34,445–36,120).
We defined large trees as those species that usually occur with
individuals >70 cm DBH or taller than 31 m as adopted by Clark
and Clark (1996), Turner (2001) and Laurance et al. (2000). These
species represent a functional group in tropical forests as they
share life-history traits: large-stemmed adults in the population,
high requirements of light (obtained via crow exposure) for
flowering and fruiting, long-life span, lower rates of recruitment
and mortality, and higher woody density as compared to other tree
guilds of tropical forests (Clark and Clark, 1992; Nascimento et al.,
2005). Finally, large tree species encompass two subsets: (1)
1912 M.A. Oliveira et al. / Forest Ecology and Management 256 (2008) 1910–1917

Fig. 1. (A) Map of northeastern Brazil, showing (B) the distribution of the Atlantic forest in the Pernambuco Center of Endemism region; the original and current distributions
of forest cover are indicated by grey and black areas, respectively. Study landscape (white rectangle, C) showing the 58 floristic plots located along forest edges, small forest
fragments, and core forest interior (dark grey polygons), including the 3500 ha Coimbra Forest (lower right). Light grey and white areas represent unsampled forest fragments
and sugar-cane monoculture, respectively. Adapted from Santos et al. (2008).

emergent tree species, those with large adults reaching the highest
forest layer; and (2) canopy species, those with the largest adults
reaching intermediate canopy layers (Tabarelli et al., 1999).
Tree species assignment into these functional groups was
carried out based on (1) an intensive tree survey conducted in Serra
Grande, including seventy-five 0.1-ha plots located in forest
fragments, forest edges, second-growth stands and forest interior
areas (Oliveira et al., 2004; Grillo et al., 2006; Santos et al., 2008);
(2) a comprehensive literature review, including books, papers,
plant monographs, and MSc and PhD dissertations (e.g., Roosma-
len, 1985; Lorenzi, 1998; Barroso et al., 1999; Ribeiro et al., 1999;
several issues of Flora Neotropica); and (3) the examination of
voucher descriptions housed in the eight major herbaria of
northeastern Brazil. These sources were further supplemented
by our own personal knowledge of the life-history traits of Atlantic
forest tree species (see Tabarelli et al., 1999; Silva and Tabarelli,
2000; Tabarelli and Mantovani, 2000; Tabarelli and Peres, 2002;
Oliveira et al., 2004; Melo et al., 2006, 2007; Santos et al., 2008).
Based on this collective information, we calculated the number and
proportion of large tree species and their stems (DBH  10 cm) for
all plots within the three habitats (i.e. forest edge, forest fragments
and forest interior). As mentioned elsewhere (Santos et al., 2008),
we are aware that the study design was limited by the landscape
configuration available to us; the Coimbra Forest does not fully
represent a ‘continuous forest’ and consists of a single, unrepli-
cated tract of forest at the landscape and regional scales. Moreover,
reduced forest cover at landscape scale greatly limited plot size and
number, as only small plots could be accommodated in small forest
fragments. Our sampling limitation contrasts with the large-scale
approach (plots 1–50 ha in size), which is frequently adopted to
examine demographic aspects of tropical trees. However, the Serra
Grande landscape is the best available contemporary scenario to
assess the long-term effects of habitat fragmentation on the
structure of Atlantic forest tree assemblages, particularly because
tree assemblages may be approaching near-equilibrium conditions
(Santos et al., 2008).
3.2. Explanatory variables
Because a number of patch and landscape-scale environmental
variables may contribute to differences in the structure of tree
assemblages (Laurance et al., 2007; Santos et al., 2008), we
explicitly considered fragment size, distance to the nearest forest
edge, the amount of core area (percentage of forest fragment areas
considering an edge effect of 50 m), and the amount of forest cover
retained in the surrounding landscape as explanatory variables for
the proportion of large tree species and their stems in forest
fragments (n = 28). Additionally, landscape-scale forest cover is
believed to be positively correlated with both overall connectivity
between patches (Gorresen and Willig, 2004) and amelioration of
edge effects (Laurance et al., 2002); therefore, it was quantified as
the percentage of forest within a 1-km external buffer set from the
perimeter of each fragment. To examine the effects of habitat type,
vegetation type and soil type on between-plot species similarity,
these baseline variables were considered as factors in ANOSIM
tests (Clarke and Gorley, 2001). We also performed a Mantel test
with weighted Spearman rank correlation to address the effect of
plot location on levels of taxonomic similarity. Straight-line
distances between plots were ln-transformed, as suggested by
Condit et al. (2002) and Jones et al. (2006), and postulated by
Hubbell (2001) neutral theory. Patch and landscape metrics were
quantified using two GIS packages (ArcView 3.2 and Erdas Imagine
8.4) on the basis of (1) three Landsat and Spot images (years 1989,
1998, 2003); (2) a set of 160 aerial photos (1:8000) taken from
helicopter overflights commissioned in April 2003; (3) digital
vegetation and soil maps (IBGE, 1985); and (4) a soil map provided
 M.A. Oliveira et al. / Forest Ecology and Management 256 (2008) 1910–1917
by the Usina Serra Grande Agriculture Office. It should be noted
that possible effects of selective logging on the size structure of
tree assemblages across habitats were not explicitly examined
here. Although this human-induced disturbance is an impacting
source of large tree mortality in tropical forests (Brown and
Gurevitch, 2004), the Serra Grande landscape has long been
protected against logging (Santos et al., 2008). This current status
of unlogged forest was confirmed by the complete lack of stumps
across both the habitats and plots inventoried in this study, via
interviews with long-term residents and company employees who
had long been in charge of forest protection, and by our own
experience in Serra Grande landscape since 2000.
3.3. Data analysis
Between-habitat differences in the proportion (i.e. relative
importance) and absolute number of large tree species and their
stems 10 cm DBH were compared via one-way ANOVA (followed
by Tukey post hoc comparisons). Stepwise multi-linear regressions
(sensu Sokal and Rohlf, 1995) were used to detect any influence of
the explanatory variables on relative importance of large tree
species and their stems within the 28 forest fragment plots. Forest
interior and forest edge plots were excluded from regressions
because they were unavoidably placed within the same large
fragment (Coimbra Forest). Explanatory variables were trans-
formed as follows: fragment size (square root transformed), plot
distance to the nearest forest edge (log transformed), amount of
forest cover (arcsine transformed), and amount of core area within
fragments (square root transformed).
In order to compare the distribution of trees (considering all
tree species) within size classes across the three habitats, we
adopted a planned comparison approach sensu Sokal and Rohlf
(1995). First, cross-habitat distributions were compared via two-
way ANOVAs assigning habitat and size classes (DBH and height)
as independent factors; i.e. one ANOVA for DBH and another for
tree height. ANOVAs were then followed by contrast analyses
which tested for differences between forest edge and forest
fragments (first comparison) and between these two habitats and
forest interior (second comparison). Percentage of trees within size
classes (dependent variables) were arcsine transformed in order to
stabilize variance, improve normality of data and consequently
increase the explanatory power of models. To infer the proximate
mechanisms of large tree erosion in the edge-affected habitats (i.e.
edges and small fragments), we also examined stem-specific DBH–
height relationships across habitats via an ANCOVA; tree-height
log was fitted to stem-DBH log (covariate) and habitat type (factor).
Finally, we performed an indicator species analysis (sensu Dufrêne
and Legendre, 1997) based on two groups of tree plots: one
consisting exclusively of forest interior plots (n = 20) and the other
group comprised of forest edge and small fragment plots (n = 38).
Analyses were carried out using Statistica 6.0 and PC-Ord 4.36
(McCune and Mefford, 1999).
4. Results
A total of 4799 living trees belonging to 198 tree species were
recorded within the 58 plots across the 3 habitats; 34 species
(17.1%) and 794 stems (16.9%) were assigned to the functional
group of large tree species, most of them as long-lived emergent
species. Edge-affected habitats were greatly impoverished in terms
of tree species: 18.4  4.5 species per plot (mean  S.D.) in forest
edges and 22.5  8.5 species in forest fragments vs. 34.8  7.7 species
in forest interior plots (F = 20.61, d.f. = 2, p < 0.0001). Edge-affected
habitats were far more impoverished in terms of large tree species as
this functional group accounted for less than 15% of all stems and tree
1913
species in these habitats, whereas they reached nearly 25% in forest
interior plots (Fig. 2). This 50% decline was highly significant for
both species and stems (F = 20.02, d.f. = 2, p < 0.0001; F = 30.5,
d.f. = 2, p < 0.0001) and resulted from the low occurrence of large
tree species in forest edges (1.8  1.1 large tree species per plot) and
forest fragments (3.5  2.8 species) as compared to forest interior
plots (9.5  2.4 species; F = 45.5, d.f. = 2, p < 0.0001). Collectively,
these scores revealed a robust decline on large tree species richness in
edge-affected habitats regardless of measurement in absolute or
relative terms. Finally, stepwise regressions detected a small but
rather significant effect of forest cover, which ranged from 0% up to
31.1%, on the proportion of large tree species (adjusted R2 = 15.3%,
F = 5.87, p = 0.023) and their stems 10 cm DBH (adjusted R2 = 14.7%,
F = 5.65, p = 0.025, n = 28).
Although large-stemmed and very tall trees were consistently
rare across habitats (see Table 1), the distribution of trees within
size classes greatly differed among habitats, and it clearly revealed
the current status of the large-tree stand in the study landscape. As
expected, forest edges and forest fragments did not differ (p = 0.84,
contrast analysis) since they were completely dominated by small
and medium-sized stems (Fig. 3) and almost completely lacked
large-stemmed trees (DBH > 70 cm); 0.24  0.27% of all stems. In
forest interior plots, stem distribution was less asymmetric and
significantly differed from edge-affected habitats (F = 17.6, d.f. = 1,
p < 0.0001). Large-stemmed trees reached 1.68  2.16% of the whole
plot stand in this habitat, a five-fold increase in comparison to edges
and small fragments. The tree distribution across height classes in
forest edges and fragments showed a drastic and similar shift towards
shorter trees; these habitats were largely dominated by those shorter
than 21 m (Fig. 4). Moreover, very tall trees (31 m height) were
completely absent from all forest edge plots and represented only
0.22  0.7% of the stems sampled in the 28 fragment plots.
Conversely, this group of trees accounted for 2.9  2.8% of all stems
recorded in forest interior plots, where distribution was more
symmetric and substantially differed from those in forest edges
and fragments (F = 4.58, d.f. = 1, p = 0.032). These remarkable
differences resulted from the dramatic rarity of large-stemmed trees
in edge-affected habitats—7 stems (0.25% of all stems, Table 1) within
2 plots (5.2%) vs. 27 large-stemmed trees distributed over 50% of
forest interior plots (G = 10.7, d.f. = 1, p = 0.002). Relative to their DBH,
forest edges and fragments supported relatively shorter trees as well
(adjusted R2 = 39.7%, F = 1046.69, p < 0.0001). Precisely, trees 10 cm
in DBH were approximately 30% shorter in comparison to forest
interior trees (Fig. 5), which implies a depressed height/diameter
Fig. 2. Average percentage (S.D.) of large tree species in terms of stems (10 cm in
DBH) and species in fifty-eight 0.1-ha plots in forest edges (n = 10), forest fragments
(n = 28) and forest interior plots (n = 20) in Serra Grande, Brazil.
1914 M.A. Oliveira et al. / Forest Ecology and Management 256 (2008) 1910–1917

Table 1
Number of tree species and stems recorded within fifty-eight 0.1-ha plots in forest
edges, forest fragments, and forest interior plots in Serra Grande, Brazil

Habitats No. of tree No. of stems No. of stems No. of trees

species 10 cm in DBH >70 cm in DBH >31 m height

Forest edge 59 601 2 0

Forest fragments 138 2125 5 6
Forest interior 154 2073 27 56

Total sampled 198 4799 34 62

ratio (a drastic change in tree architecture) and an evident

simplification/loss of forest vertical structure in edge-affected
habitats.
Therefore, forest edges exhibited the largest differences
compared to forest interior plots in terms of the size structure
of tree assemblages despite the fact that these two habitats
were embedded within the same large remnant (Coimbra Forest)
and separated by shorter distances; edge and forest interior
plots were on average 2480.4 m  960.2 m apart (n = 200 random
pairs), whereas forest fragment and forest interior plots were
20,373.9 m  3836.28 m apart (n = 200 random pairs). This finding
reinforces our assumption that both historical and contemporary
logging has not structured tree assemblages; it is unreasonable to
suppose that logging completely eroded the vertical structure of
Coimbra forest edges, but saved large trees only 200 m apart in forest
interior areas.
ANOSIM uncovered no significant correlation between soil type
and degree of taxonomic similarity between plots (R = 0.102;
p = 0.987), but detected a small effect of vegetation type (R = 0.38;
p = 0.01) and a stronger effect of habitat type (R = 0.706; p = 0.01).
Tree community structure in forest interior plots was significantly
different from that along edge (R = 0.934; p = 0.01) and those in
small fragments (R = 0.79; p = 0.01). This was confirmed by a
Mantel test, which failed to uncover any large-scale spatial effect
on the taxonomic similarity across the 58 plots (Rho = 0.329;
p = 0.99). Finally, an indicator species analysis yielded a set of 12
large tree species, including emergent, long-lived pioneer, hard
and softwood timber species (e.g. Virola, Lecythis, Manilkara,
Aspidosperma genera), which were significantly associated with
forest interior plots (Table 2). In contrast, forest edges and
fragments (edge-affected habitats) lacked any large tree species
serving as indicator of these altered habitats.
Fig. 4. Average percentage (S.D.) of trees (10 cm in DBH) within seven classes of
height in fifty-eight 0.1-ha plots in forest edges (n = 10), forest fragments (n = 28) and
forest interior plots (n = 20) in Serra Grande, Brazil.
5. Discussion
Our findings revealed a substantial shift in the size structure of
tree assemblages and the impoverishment of the large-tree stand
in an aging, hyper-fragmented landscape. Such erosion refers to a
robust decline of large tree species richness (in relative and
absolute terms), reduced abundance of large-stemmed and very
tall trees (a distorted size structure), and the complete elimination
of indicator emergent species in edge-affected habitats. In fact, the
abundance of large trees in the edge-affected habitats of the Serra
Grande landscape was far lower than the scores reported for
undisturbed tracts of lowland tropical forests (including Coimbra
Forest), where this group usually represents 1–6% of all tree stems
10 cm DBH (Clark and Clark, 1996). Increased mortality of large
trees resulting from forest fragmentation has been reported,
particularly close to forest edges (Laurance et al., 2000). A recent
study (Santos et al., 2008) also reported a sharp decrease in the
richness of emergent tree species in edge-affected habitats of the
Serra Grande landscape. However, by examining tree distribution
within size classes we were able to accurately document the
floristic erosion faced by the large-tree stand in these habitats,

Fig. 3. Average percentage (S.D.) of trees (10 cm in DBH) within seven classes of Fig. 5. Average tree height (0.95 confidence interval), considering an average stem–
DBH in fifty-eight 0.1-ha plots in forest edges (n = 10), forest fragments (n = 28) and DBH of 19.6 cm (the average DBH for the whole tree stand) in forest edges, forest
forest interior plots (n = 20) in Serra Grande, Brazil. fragments and forest interior plots in Serra Grande, Brazil. n = 4799 stems.
 M.A. Oliveira et al. / Forest Ecology and Management 256 (2008) 1910–1917 1915

Table 2
Indicator tree species (sensu Dufrêne and Legendre, 1997) recorded in 20 forest interior plots in the Coimbra Forest, with their respective families, regeneration strategies and
indicator values (IV) at Usina Serra Grande, Brazil

Indicator species Family R. strategya IV Randomized IV p

Virola gardneri Myristicaceae S-tolerant 87.7 29.1  6.1 0.001

Manilkara salzmanii Sapotaceae S-tolerant 45.9 19  5.3 0.001
Balizia pedicellaris Fabaceae LL pioneer 38.8 17.2  5.0 0.006
Sloanea obtusifolia Elaeocarpaceae S-tolerant 37.3 15  4.5 0.001
Diplotropis purpurea Fabaceae S-tolerant 36.3 20.7  6.2 0.02
Ficus guaranitica Moraceae LL pioneer 34.2 18.3  4.9 0.011
Sloanea guianensis Elaeocarpaceae S-tolerant 33.4 14  4.8 0.004
Couepia rufa Chrysobalanaceae S-tolerant 32 20.6  5.1 0.045
Pterocarpus violaceus Fabaceae LL pioneer 30.6 16.2  4.7 0.009
Aspidosperma spruceanum Apocynaceae LL pioneer 30 11.5  4.3 0.001
Aspidosperma discolor Apocynaceae LL pioneer 25 10  3.9 0.007
Pradozia lactescens Sapotaceae S-tolerant 25 10  3.9 0.011
a
S-tolerant = shade tolerant; LL pioneer = long-lived pioneer.

including the structural collapse of the forest emergent layer in the
edge of the largest and best preserved forest remnant of northeast
Brazil. This marked pattern emerged despite our relatively reduced
sample effort and cannot be explained by either baseline variables
(e.g. vegetation and soil type) or plot spatial location.
Therefore, our findings represent a consistent set of empirical
evidence for a persistent impoverishment of the large-tree stand
associated with the establishment of aging, hyper-fragmented
landscapes, in which edge-affected habitats prevail. They also
indicate that many floristic and structural trends documented in
more recently fragmented forest landscapes, such as those in the
central Brazilian Amazonia (see Laurance et al., 2000), represent the
first steps towards a more drastic and pervasive simplification of
forest vertical structure. However, the forces promoting the shifts
documented here are not completely understood. Some investiga-
tions have observed elevated mortality of large trees due to
uprooting driven by increased windshear and turbulence near forest
edges, i.e. a mechanical force as an agent of tree death (D’Angelo
et al., 2004). Physiological stress imposed by edge-related micro-
climatic changes has also been proposed as an additional source of
increased mortality among large trees (Laurance et al., 2000;
Nascimento and Laurance, 2004), but this mechanism still lacks
empirical support. In addition to these edge-induced sources, large
canopy and emergent trees are particularly susceptible to selective
logging (Brown and Gurevitch, 2004), droughts (Nepstad et al.,
2007), and delayed mortality induced by surface fires (Barlow et al.,
2003; Barlow and Peres, 2008). Logging and fire, in fact, are likely to
rival fragmentation-induced processes as the major forces leading
large tree populations to collapse (extinction filters) in intensively
human exploited landscapes (see Nepstad et al., 1999).
Our study site consisted of an aging, hyper-fragmented
landscape in which the impoverishment/collapse of large-tree
stands had probably occurred a long time ago. Although this
scenario provides an interesting opportunity to investigate long-
term effects of habitat fragmentation, it does not permit a proper
investigation of the proximate causes of large tree mortality, as
most of these trees have already succumbed in edge-affected
habitats; standing-dead large trees were inexpressive across
habitats. However, some findings in this landscape apparently
support the wind damage hypothesis. Large tree species in Serra
Grande positively correlated with the amount of forest cover
around fragments. Furthermore, trees inhabiting edge-affected
habitats were drastically shorter (relative to their DBH) than those
in forest interior areas. Depressed height/diameter ratio has long
been accepted as resulting from plant acclimation to better
withstand increased wind loading and its impacts (Ennos, 1997;
Read and Stokes, 2006; Zenner, 2008), as stem mechanical safety
decreases with increasing height/diameter ratio (van Gelder et al.,
2006). Chronic wind stress in fact not only shapes tree architecture
(including tropical trees), but also the size structure of tree
assemblages across tropical and temperate regions (Webb et al.,
1999). It appears that those Serra Grande fragments buffered
against wind loading/disturbance (via increased surrounding
forest cover) are more able to retain large trees established prior
to fragmentation; but also provide suitable conditions for the
recruitment of new ones as growing, young trees are less exposed
to winds. This rationale is highly consistent with and reinforces the
notion that the more closely the matrix resembles the structure of
forest fragments the less pronounced are the edge effects
(Mesquita et al., 1999; Harper et al., 2005).
In synthesis, this paper outlines some noticeable shifts in the
size structure of tree assemblages in response to habitat
fragmentation, including the floristic impoverishment of the
large-tree stand in edge-affected habitats. Despite the relative
lack of knowledge about the mechanisms that make edges and
small fragments hostile to large tree species, our findings reinforce
the notion that edge-dominated, hyper-fragmented landscapes
tend to retain degenerated/altered tree assemblages (sensu Santos
et al., 2008). Furthermore, this impoverishment is likely to trigger
devastating impacts, via extinction cascades, across other func-
tional/taxonomic groups, which require resources exclusively
provided by large trees. In the Atlantic forest of northeast Brazil, for
instance, the illuminated crowns of large trees offer an irreplace-
able habitat for at least two-dozen species of bromeliads (nearly a
quarter of the bromeliad flora in this region), which exclusively
inhabit the sun-exposed crowns positioned in the forest emergent
layer (Siqueira-Filho and Tabarelli, 2006). By retaining only edge-
affected habitats, severely fragmented landscapes face a severe
threat of biodiversity loss, which clearly impairs their eligibility as
future conservation targets and degrade their potential value in
terms of ecosystem services and economic opportunities (sensu
Zarin, 2004). This clearly weakens the justification to avoid further
deforestation in already severely fragmented Atlantic forest
landscapes; one of the most endangered global hotspots of
biodiversity (Myers et al., 2000). We hope that our findings
encourage wider-scale studies addressing the whole set of
proximate mechanisms leading the impoverishment of the
large-tree stand, particularly in edge-affected habitats. This is a
crucial step towards the definition of land-use regulations and
conservation guidelines designed to avoid a persistent degradation
of hyper-fragmented landscapes.
Acknowledgments
We are enormously grateful to Alexandre Grillo for making his
tree database available for the authors; Luis Antônio Bezerra and
1916 M.A. Oliveira et al. / Forest Ecology and Management 256 (2008) 1910–1917
José Clodoaldo Bakker for authorizing our fieldwork at the Usina
Serra Grande landholding; CNPq (research grant to M. Tabarelli),
Fundação O Boticário de Proteção à Natureza; and Conservação
Internacional for essential financial support. Two anonymous
referees offered constructive criticisms on the manuscript.
References
Aide, T.M., Grau, H.R., 2004. Ecology, globalization, migration, and Latin American
ecosystems. Science 305, 1915–1916.
Barlow, J., Peres, C.A., 2008. Fire-mediated dieback and compositional cascade in an
Amazonian forest. Phil. Trans. R. Soc. B 363, 1787–1794.
Barlow, J., Peres, C.A., Lagan, B.O., Haugaasen, T., 2003. Large tree mortality and the
decline of forest biomass following Amazonian wildfires. Ecol. Lett. 6, 6–8.
Barroso, G.M., Morim, M.P., Peixoto, A.L., Ichaso, C.L.F., 1999. Frutos e Sementes:
Morfologia Aplicada à Sistemática de Dicotiledôneas. Universidade Federal de
Viçosa, Viçosa.
Brokaw, N.V.L., 1982. Treefalls: frequency, timing, and consequences. In: Leigh, Jr.,
E.G., Rand, A.S., Windsor, D.M. (Eds.), The Ecology of a Tropical Forest: Seasonal
Rhythms and Long-Term Changes. Smithsonian Institution Press, Washington,
DC, USA, pp. 101–108.
Brown, K.A., Gurevitch, J., 2004. Long-term impacts of logging on forest diversity in
Madagascar. Proc. Natl. Acad. Sci. U.S.A. 101, 6045–6049.
Castilho, C.V., Magnusson, W.E., Araújo, R.N.O., Luizão, R.C.C., Luizão, F.J., Lima, A.P.,
Higuchi, N., 2006. Variation in aboveground tree live biomass in a central
Amazonian forest: Effects of soil and topography. Forest Ecol. Manage. 234,
85–96.
Chambers, J.Q., Higuchi, N., Schimel, J.P., 1998. Ancient trees in Amazonia. Nature
391, 135–136.
Chambers, J.Q., Santos, J., Ribeiro, R.J., Higuchi, N., 2001. Tree damage, allometric
relationships, and above-ground net primary production in central Amazon
forest. Forest Ecol. Manage. 152, 73–84.
Clark, D.A., Clark, D.B., 1992. Life history diversity of canopy and emergent trees in a
neotropical rain forest. Ecol. Monogr. 62, 315–344.
Clark, D.B., Clark, D.A., 1996. Abundance, growth and mortality of very large trees in
neotropical lowland rain forest. Forest Ecol. Manage. 80, 235–244.
Clarke, K.R., Gorley, R.N., 2001. PRIMER v5: User Manual/Tutorial. PRIMER-E Ltd,
Playmouth.
Condit, R., Pitman, N., Leigh, E.G., Chave, J., Terborgh, J., Foster, R., Núñez, P.V.,
Aguilar, S., Valencia, R., Gorky, V., Muller-Landau, H.C., Losos, E., Hubbell, S.,
2002. Beta-diversity in tropical forest trees. Science 295, 666–669.
Curran, L.M., Leighton, M., 2000. Vertebrate responses to spatiotemporal variation
in seed production of mast-fruiting Dipterocarpaceae. Ecol. Monogr. 70, 101–
128.
D’Angelo, S.A., Andrade, A.C.S., Laurance, S.G., Laurance, W.F., Mesquita, R.C.G., 2004.
Inferred causes of tree mortality in fragmented and intact Amazonian forests. J.
Trop. Ecol. 20, 243–246.
Delannoy, C.A., Tossas, A.G., 2002. Breeding biology and nest site characteristics of
Puerto Rican Broad-winged Hawks at the Rio Abajo Forest. Caribb. J. Sci. 38, 20–26.
Dufrêne, M., Legendre, P., 1997. Species assemblages and indicator species: the need
for a flexible asymmetrical approach. Ecol. Monogr. 67, 645–666.
Ennos, A.R., 1997. Wind as an ecological factor. Trends Ecol. Evol. 12, 108–111.
Gascon, C., Williamson, B., Fonseca, G.A.B., 2000. Receding forest edges and vanish-
ing reserves. Science 288, 1356–1358.
Girão, L.C., Lopes, A.V., Tabarelli, M., Bruna, E.M., 2007. Changes in tree reproductive
traits reduce functional diversity in a fragmented Atlantic forest landscape.
PLoS One 9, e908.
Gorresen, P.M., Willig, M.R., 2004. Landscape responses of bats to habitat fragmen-
tation in Atlantic forest of Paraguay. J. Mammal. 85, 688–697.
Gribel, R., Gibbs, P.E., Queiróz, A.L., 1999. Flowering phenology and pollination
biology of Ceiba pentandra (Bombacaceae) in Central Amazonia. J. Trop. Ecol. 15,
247–263.
Grillo, A.S., Oliveira, M.A., Tabarelli, M., 2006. Árvores. In: Pôrto, C., Almeida-Cortez,
J.S., Tabarelli, M. (Eds.), Diversidade Biológica e Conservação da Floresta Atlân-
tica ao Norte do Rio São Francisco. Série Biodiversidade no. 14. Ministério do
Meio Ambiente, Brası́lia, pp. 191–216.
Harper, K.A., MacDonald, S.E., Burton, P.J., Chen, J., Brosofske, K.D., Saunders, S.C.,
Euskirchen, E., Roberts, D., Jaiteh, M.S., Per-Anders, E., 2005. Edge influence on
forest structure and composition in fragmented landscapes. Conserv. Biol. 19,
768–782.
Hubbell, S.P., 2001. The unified theory of biodiversity and biogeography. Mono-
graphs in Population Biology, vol. 32. Princeton University Press, Princeton.
IBGE, 1985. Atlas Nacional do Brasil: Região Nordeste. IBGE, Rio de Janeiro.
Jones, M.M., Tuomisto, H., Clark, D.B., Olivas, P., 2006. Effects of mesoscale envir-
onmental heterogeneity and dispersal limitation of floristic variation in rain
forest ferns. J. Ecol. 94, 181–195.
Laurance, W.F., 2001. Fragmentation and plant communities: synthesis and impli-
cations for landscape management. In: Bierregaard, Jr., R.O., Gascon, C., Love-
joy, T.E., Mesquita, R.C.G. (Eds.), Lessons from Amazonia: the Ecology and
Conservation of a Fragmented Forest. Yale University Press, New Haven, pp.
158–168.
Laurance, W.F., Delamonica, P., Laurance, S.G., Vasconcelos, H.L., Lovejoy, T.E., 2000.
Rainforest fragmentation kills big trees. Nature 404, 836–1836.
Laurance, W.F., Lovejoy, L.E., Vasconcelos, H.L., Bruna, E.M., Didham, R.K., Stouffer,
P.C., Gascon, C., Bierregaard Jr., R.O., Laurance, S.G., Sampaio, E., 2002. Ecosystem
decay of Amazonian forest fragments: a 22-year investigation. Conserv. Biol. 16,
605–618.
Laurance, W.F., Nascimento, H.E.M., Laurance, S.G., Andrade, A., Ribeiro, J.E.L.S.,
Giraldo, G.P., Lovejoy, T.E., Condit, R., Chave, J., Harms, K.E., D‘Ângelo, S., 2006.
Rapid decay of tree-community composition in Amazonian forest fragments.
Proc. Natl. Acad. Sci. U.S.A. 103, 19010–19014.
Laurance, W.F., Nascimento, H.E.M., Laurance, S.G., Andrade, A., Ewers, R.M., Harms,
K.E., Luizão, R.C.C., Ribeiro, J.E., 2007. Habitat fragmentation, variable edge
effects, and the landscape divergence hypothesis. PloS One 10, e1017.
Lorenzi, H., 1998. Árvores Brasileiras: Manual de Identificação e Cultivo de Plantas
Arbóreas Nativas do Brasil, vols.1 and 2. Editora Plantarum, Nova Odessa.
Lowman, M.D., Nadkarni, N.M., 1995. Forest Canopies. Academic Press, New York.
McCune, B., Mefford, M.J., 1999. PC-ORD: Multivariate Analysis of Ecological Data,
Version 4.36. MjM Software, Gleneden Beach, OR, U.S.A.
Melo, F.P.L., Dirzo, R., Tabarelli, M., 2006. Biased seed rain in forest edges: evidence
from the Brazilian Atlantic forest. Biol. Conserv. 132, 50–60.
Melo, F.P.L., Lemire, D., Tabarelli, M., 2007. Extirpation of large-seeded seedlings from
the edge of a large Brazilian Atlantic forest fragment. Écoscience 14, 124–129.
Mesquita, R.C.G., Delamônica, P., Laurance, W.F., 1999. Effects of surrounding
vegetation on edge-related tree mortality in Amazonian forest fragments. Biol.
Conserv. 91, 129–134.
Michalski, F., Nishi, I., Peres, C.A., 2007. Disturbance-mediated drift in tree func-
tional groups in Amazonian forest fragments. Biotropica 39, 691–701.
Myers, N., Mittermeier, R.A., Mittermeier, C.G., Fonseca, G.A.B., Kent, J., 2000.
Biodiversity hotspots for conservation priorities. Nature 403, 845–853.
Nascimento, H.E.M., Laurance, W.F., 2004. Biomass dynamics in Amazonian forest
fragments. Ecol. Appl. 14 (Suppl.), 127–138.
Nascimento, H.E.M., Laurance, W.F., Condit, R., Laurance, S.G., D’Angelo, S., Andrade,
A.C., 2005. Demographic and life-history correlates for Amazonian trees. J. Veg.
Sci. 16, 625–634.
Nepstad, D.C., Tohver, I.M., Ray, D., Moutinho, P., Cardinot, G., 2007. Mortality of
large trees and lianas following experimental drought in Amazon forest.
Ecology 88, 2259–2269.
Nepstad, D.C., Verı́ssimo, A., Alencar, A., Nobre, C., Lima, E., Lefebvre, P., Schlesinger, P.,
Potter, C., Moutinho, P., Mendoza, E., Cochrane, M., Brooks, V., 1999. Large-scale
impoverishment of Amazon forests by logging and fire. Nature 398, 505–508.
Newbery, D.M., Chuyong, G.B., Zimmermann, L., 2006. Mast fruiting of large
ectomycorrhizal African rain forest trees: importance of dry season intensity,
and the resource-limitation hypothesis. New Phytol. 170, 561–579.
Oliveira, A.A.D., Mori, S.A., 1999. A central Amazonian terra firme forest. I. High tree
species richness on poor soils. Biodivers. Conserv. 8, 1219–1244.
Oliveira, M.A., Grillo, A.S., Tabarelli, M., 2004. Forest edge in the Brazilian Atlantic
forest: drastic changes in tree species assemblages. Oryx 38, 389–394.
Peres, C.A., 2000. Identifying keystone species plant resources in tropical forests:
the case of gums from Parkia pods. J. Trop. Ecol. 16, 287–317.
Poonswad, P., 1995. Nest-site characteristics of 4 sympatric species of hornbills in
Khao-Yai National Park, Thailand. J. Trop. Ecol. 137, 183–191.
Pôrto, C., Almeida-Cortez, J.S., Tabarelli, M., 2006. Diversidade Biológica e Conser-
vação da Floresta Atlântica ao Norte do rio São Francisco. Série Biodiversidade
no. 14. Ministério do Meio Ambiente, Brası́lia.
Primack, R.B., Corlett, R., 2005. Tropical Rain Forests: An Ecological and Biogeo-
graphical Comparison. Blackwell Publishing, New York.
Putz, F.E., 1983. Treefall pits and mounds, buried seeds, and the importance of soil
disturbance to pioneer trees on Barro Colorado Island. Panama Ecol. 64, 1069–
1074.
Read, J., Stokes, A., 2006. Plant biomechanics in an ecological context. Am. J. Bot. 93,
1546–1565.
Ribeiro, J.E.L.S., Hopkins, M.J.G., Vicentini, A., Sothers, C.A., Costa, M.A.S., Brito, J.M.,
Souza, M.A.D., Martins, L.H.P., Lohmann, L.G., Assunção, P.A.C.L., Pereira, E.C.,
Silva, C.F., Mesquita, M.R., Procópio, L.C., 1999. Flora da Reserva Ducke: Guia de
Identificação de uma Floresta de Terra-Firme na Amazônia Central. INPA-DFID,
Manaus.
Roosmalen, M.G.M.van, 1985. Fruits of the Guianan Flora. Institute of Systematic
Botany, Utrecht.
Santos, B.A., Peres, C.A., Oliveira, M.A., Grillo, A., Alves-Costa, C.P., Tabarelli, M., 2008.
Drastic erosion in functional attributes of tree assemblages in Atlantic forest
fragments of northeastern Brazil. Biol. Conserv. 141, 249–260.
Silva, J.M.C., Tabarelli, M., 2000. Tree species impoverishment and the future flora of
the Atlantic forest of northeast Brazil. Nature 404, 72–73.
Siqueira-Filho, J.A., Tabarelli, M., 2006. Bromeliad species from the Atlantic forest of
north-east Brazil: losses of critical populations of endemic species. Oryx 40,
218–224.
Small, A., Martin, T.G., Kitching, R.L., Wong, K.M., 2004. Contribution of tree species
to the biodiversity of a 1 ha Old World rainforest in Brunei. Borneo. Biodivers.
Conserv. 13, 2067–2088.
Sokal, R.R., Rohlf, F.J., 1995. Biometry. Freeman and Company, New York.
Stoner, K.E., Vulinec, K., Wright, S.J., Peres, C.A., 2007. Hunting and plant community
dynamics in tropical forests: a synthesis and future directions. Biotropica 39,
385–392.
Tabarelli, M., Mantovani, W., 2000. Gap-phase regeneration in a tropical montane
forest: the effects of gap structure and bamboo species. Plant Ecol. 148, 149–155.
Tabarelli, M., Peres, C.A., 2002. Abiotic and vertebrate seed dispersal in the Brazilian
Atlantic forest: implications for forest regeneration. Biol. Conserv. 106, 165–176.
 M.A. Oliveira et al. / Forest Ecology and Management 256 (2008) 1910–1917
Tabarelli, M., Mantovani, W., Peres, C.A., 1999. Effects of habitat fragmentation and
plant guild structure in the montane Atlantic forest of southeastern Brazil. Biol.
Conserv. 91, 119–127.
Turner, I.M., 2001. The Ecology of Trees in the Tropical Rain Forest. Cambridge
University Press, Cambridge.
Turner, I.M., Corlett, R.T., 1996. The conservation value of small, isolated fragments
of lowland tropical rain forest. Trends Ecol. Evol. 11, 330–333.
van Gelder, H.A., Poorter, L., Sterck, F.J., 2006. Wood mechanics, allometry, and life-
history variation in a tropical rain forest tree community. New Phytol. 171, 367–
378.
Veloso, H.P., Rangel-Filho, A.L.R., Lima, J.C.A., 1991. Classificação da Vegetação
Brasileira Adaptado a um Sistema Universal. IBGE, Rio de Janeiro.
Vieira, S., Camargo, P.B., Selhorst, D., Silva, R., Hutyra, L., Chambers, J.Q., Brown, I.F.,
Higuchi, N., Santos, J., Wofsy, S.C., Trumbore, S.E., Martinelli, L.A., 2004. Forest
structure and carbon dynamics in Amazonian tropical rain forests. Oecologia
140, 468–479.
1917
Webb, E.L., Stanfield, B.J., Jensen, M.L., 1999. Effects of topography on rainforest tree
community structure and diversity in American Samoa, and implications for
frugivore and nectarivore populations. J. Biogeogr. 26, 887–897.
Whitmore, T.C., 1998. An Introduction to Tropical Rain Forests, 2nd edition. Oxford
University Press, Oxford.
Wright, S.J., 2005. Tropical forests in a changing environment. Trends Ecol. Evol. 20,
553–560.
Wright, S.J., Muller-Landau, H.C., 2006. The future of tropical forest species. Bio-
tropica 38, 287–301.
Zarin, D.J., 2004. Neotropical working forests: concepts and realities. In: Zarin,
D.J., Alavalapati, J.R.R., Putz, F.E., Schmink, M. (Eds.), Working Forests in the
Neotropics: Conservation Through Sustainable Management? Columbia Uni-
versity Press, New York, pp. 1–12.
Zenner, E.K., 2008. Short-term changes in Pinus strobus sapling height/diameter
ratios following partial release: testing the acclimative stem-form development
hypothesis. Can. J. Forest Res. 38, 181–189.