B I O L O G I CA L C O N S E RVAT I O N 1 4 1 ( 2 0 0 8 ) 2 4 9 –2 6 0

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journal homepage: www.elsevier.com/locate/biocon

Drastic erosion in functional attributes of tree assemblages

in Atlantic forest fragments of northeastern Brazil

Bráulio A. Santosa, Carlos A. Peresb, Marcondes A. Oliveirac, Alexandre Grilloc,

Cecı́lia P. Alves-Costac, Marcelo Tabarellic,*
a
Biological Dynamics of Forest Fragment Project, National Institute for Amazonian Research (INPA), C.P. 478, Manaus,
AM 69011-970, Brazil
b
School of Environmental Sciences, University of East Anglia, Norwich NR4 7TJ, UK
c
Departamento de Botânica, Universidade Federal de Pernambuco, Recife, PE 50670-901, Brazil

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

Article history: The long-term dynamics of plant communities remain poorly understood in isolated trop-
Received 3 May 2007 ical forest fragments. Here we test the hypothesis that tropical tree assemblages in both
Received in revised form small forest fragments and along forest edges of very large fragments are functionally
31 August 2007 much more similar to stands of secondary growth (5–65-yr old) than to core primary forest
Accepted 18 September 2007 patches. The study was carried out in a severely fragmented landscape of the Brazilian
Available online 5 November 2007 Atlantic forest. Nine functional attributes of tree assemblages were quantified by sampling
all trees (DBH P 10 cm) within 75 plots of 0.1 ha distributed in four forest habitats: small
Keywords: forest fragments (3.4–79.6 ha), forest edges, second-growth patches, and primary forest
Edge effects interior areas within a large forest fragment (3500 ha). These habitats were markedly differ-
Forest regeneration ent in terms of tree species richness, and in the proportion of pioneer, large-seeded, and
Habitat fragmentation emergent species. Age of second-growth stands explained between 31.4% and 88.2% of
Species richness the variation in the functional attributes of tree assemblages in this habitat. As expected,
Trees most traits associated with forest edges and small forest fragments fell within the range
shown by early (<25-yr old) and intermediate-aged secondary forest stands (25–45-yr old).
In contrast to habitat type, tree assemblage attributes were not affected by vegetation type,
soil type and the spatial location of plots. An ordination analysis documented a striking flo-
ristic drift in edge-affected habitats. Our results suggest that conservation policy guidelines
will fail to protect aging, hyper-fragmented landscapes from drastic impoverishment if the
remaining forest patches are heavily dominated by edge habitat.
 2007 Elsevier Ltd. All rights reserved.

1. Introduction rance et al., 2000), understorey (Tabarelli et al., 1999), and

Habitat loss and fragmentation can drastically alter the struc-
ture and composition of tropical tree assemblages (Laurance,
2001). Forest edges and even central portions of small forest
fragments are expected to exhibit species-poor tree commu-
nities and may be impoverished in terms of emergent (Lau-
hardwood or old-growth tree species (Michalski et al., 2007).
Large-seeded trees dispersed by vertebrates, particularly
medium to large-bodied frugivores, appear to be vulnerable
to population collapse (Cordeiro and Howe, 2001; Melo et al.,
2006; Terborgh and Nuñez-Iturri, 2006). Other tree functional
groups may also be poorly represented in edge-affected

* Corresponding author: Tel.: +55 081 2126 8945; fax: +55 081 2126 8348.
E-mail address: mtrelli@ufpe.br (M. Tabarelli).
0006-3207/$ - see front matter  2007 Elsevier Ltd. All rights reserved.
doi:10.1016/j.biocon.2007.09.018
250 B I O L O G I C A L C O N S E RVAT I O N
habitats, including species sensitive to habitat desiccation
(Ferreira and Laurance, 1997), fire disturbance (Cochrane
and Laurance, 2002) and competition with vines and ruderal
species (Scariot, 2001; D’Angelo et al., 2004). Consequently, se-
verely fragmented landscapes reduced to archipelagos of
small forest fragments are likely to retain but a small, non-
random subset of species from the original source flora (Lau-
rance, 2001; Tabarelli and Gascon, 2005). However, the extent
to which habitat fragmentation depletes plant populations
and truncates the composition of plant assemblages remains
poorly understood based on either natural or controlled
experiments (see Hobbs and Yates, 2003; Aguilar et al., 2006;
Wirth et al., 2007).
One of the most conspicuous features of tree assemblages
along forest edges is the elevated abundance and richness of
fast-growing pioneer species. Pioneer species account for only
2–3% of tree species richness in continuous forest plots in
central Amazonia, but represent over a quarter of the species
richness and three times the abundance in forest fragments
1–100 ha in size after 13–17 years of isolation (Laurance
et al., 2006a). Some pioneers rapidly increase their abundance
in forest edges by over 1000%, although others either remain
constant or decline in abundance (Laurance et al., 2006a,b).
Pioneer-dominated tree assemblages or over proliferation of
pioneers have also been documented in stable Atlantic forest
edges in fragments that are at least 60-yr old (Tabarelli et al.,
1999; Oliveira et al., 2004; Grillo, 2005), suggesting that such
assemblages may be approaching near-equilibrium condi-
tions, rather than represent transient successional stages.
In edge-dominated habitats, proliferation of pioneer spe-
cies occur in parallel with phytomass collapse (Laurance
et al., 1997), suggesting that assemblages comprised primarily
of old-growth, high wood-density trees have been replaced by
second-growth or regenerating vegetation (Gascon et al.,
2000). Indeed, elevated abundance of pioneer species is a typ-
ical feature of early secondary forests younger than 25–30 yrs
following slash-and-burn agriculture (sensu Uhl, 1987) or
other disturbance events such as large treefall gaps (Brown
and Lugo, 1990; Tabarelli and Mantovani, 2000; Howorth and
Pendry, 2006). Rates of forest regeneration and other assem-
blage-level properties of young secondary forests are largely
affected by environmental constraints on tree species estab-
lishment such as diaspore availability (Nepstad et al., 1996;
Vieira et al., 2006), seed and seedling predation (Uhl, 1987),
soil infertility (Ganade and Brown, 2002), and competition
with grasses and ruderal species (Hooper et al., 2005). Early
secondary forests are therefore not homogeneous at any spa-
tial scale (Richards, 1996), but provide suitable habitat for only
a biased and impoverished subset of tree species, particularly
small-seeded pioneers (Aide et al., 2000; Guariguata and
Ostertag, 2001; Tabarelli and Peres, 2002; Martı́nez-Garza
et al., 2005). Furthermore, because secondary forests are dom-
inated by pioneer species sharing a similar set of traits
regardless of their taxonomic affinities (Whitmore, 1991; Rich-
ards, 1996; Turner, 2001), these assemblages are expected to
sustain only a small suite of tree life-history traits found in
old-growth forests.
The Atlantic forest of northeast Brazil is now reduced to
less than 6% of its original pre-Colombian extent with high
levels of forest fragmentation going back to the 16th century
1 4 1 ( 2 0 0 8 ) 2 4 9 –2 6 0
(Galindo-Leal and Câmara, 2003). Habitat loss and fragmenta-
tion are so striking that 48% of the remaining fragments in
this region are <10 ha and very few are >1000 ha (Ranta
et al., 1998). Old primary forest fragments surrounded by a
homogeneous matrix of sugar-cane plantations offer an
excellent opportunity to examine the long-term effects of
habitat fragmentation on the functional composition of stabi-
lizing tree assemblages. Here we ask whether habitat frag-
mentation in an Atlantic forest landscape can effectively
promote functional convergence of tree assemblages between
forest edges, old-growth forest and early second-growth
stands following a known history of slash-and-burn agricul-
ture. In particular, we test the hypothesis that tree assem-
blages along forest edges and in small forest fragments are
much more similar to those of secondary forest stands (5–
65-yr old) than to those of forest interior conditions in an
exceptionally large fragment. First, we compare nine struc-
tural and functional attributes of tree assemblages in these
four forest habitats, including species richness and the rela-
tive species contribution to different ecological groups of
regeneration strategy, vertical stratification, seed dispersal
mode, and seed size. Second, we document levels of taxo-
nomic similarity between habitats based on ordination anal-
ysis, and identify indicator tree species. Finally, we discuss
the processes driving changes in tree assemblages within
aging forest fragments, and their implications for biodiversity
persistence in fragmented landscapes.
2. Methods
2.1. Study landscape
This study was conducted at Usina Serra Grande, a large, pri-
vate sugar company located in the State of Alagoas, north-
eastern Brazil (830 0 S, 3550 0 W; Fig. 1). This landholding still
retains approximately 9000 ha of forest assigned to a unique
biogeographic region of the Atlantic forest, the Pernambuco
Center of Endemism (Santos et al., 2007). We selected a large
(667 km2), severely fragmented landscape containing 109 for-
est fragments (range in size = 1.67–3500 ha), all of which en-
tirely surrounded by a uniform, stable and inhospitable
matrix of sugar-cane monoculture. The Serra Grande land-
scape is located on a low-altitude plateau (300–400 m above
sea level) containing two similar classes of dystrophic soils
with high clay fractions: yellow-red latosols and yellow-red
podzols, according to the Brazilian soil classification system
(IBGE, 1985). Annual rainfall is 2000 mm, with a 3-month
dry season (<60 mm/month) from November to January. The
predominantly lowland terra firme forest included two physi-
ognomic subtypes: evergreen and semi-deciduous forests
(Veloso et al., 1991). On a regional scale, the Leguminosae,
Lauraceae, Sapotaceae, Chrysobalanaceae and Lecythidaceae
account for most tree species (Grillo et al., 2006).
Sugar-cane cultivation at Serra Grande, which dates back
to the 19th century, provided the strongest incentive for clear-
ing large tracts of pristine old-growth forests. Only 9.2% of for-
est cover is left, including the 3500-ha Coimbra Forest – the
largest and best preserved forest patch in the region. Coimbra
still retains a full complement of plant species and many of
the vertebrate groups typical of vast undisturbed tracts of
 B I O L O G I C A L C O N S E RVAT I O N 1 4 1 ( 2 0 0 8 ) 2 4 9 –2 6 0 251

Fig. 1 – Map of the Usina Serra Grande landscape of northeastern Brazil (A) showing the location of 75 plots of 0.1 ha sampled
to describe structural and functional attributes of tree assemblages in forest edges, small forest fragments, secondary forest
patches and core primary forest interior. The white rectangle in inset (B) is amplified in (C). Dark shaded polygons represent
forest fragments sampled; light-shaded and white areas, represent remaining Atlantic forest remnants that were not
sampled and a uniform matrix of sugar-cane monoculture, respectively.

Atlantic forest, such as large-seeded trees and large frugivo-
rous birds (see Chiarello, 1999; Silva and Tabarelli, 2000; Tabar-
elli and Peres, 2002; Galetti et al., 2006). However, large
mammals such as tapirs and white-lipped peccaries have
been extirpated throughout the region due to overhunting
(Silva and Tabarelli, 2000). To ensure watershed protection
and water supply for sugar-cane irrigation, the Coimbra Forest
and most other forest fragments remaining in this landscape
have been strictly protected against disturbances such as
wildfires and logging (J.C. Bakker, pers. comm.), which can
mask fragmentation-related effects (Santos et al., 2006). This
has guaranteed the spatial stability of forest fragment borders
and consequently the occurrence of both reproductive pio-
neer and shade-tolerant trees along post-closure forest edges
(Melo et al., 2006). Selection of forest sites sampled in this
landscape was based on helicopter overflights and 160 aerial
photos which were used to produce a 1:8,000 digital vegeta-
tion map (see also Section 2.4). Based on these data, a large
set of fragments retained to protect the watershed of 56 small
hydroelectric reservoirs were considered to be unsuitable be-
cause these artificial lakes may affect local microclimatic
conditions.
The Serra Grande landscape therefore provides a rare
opportunity for Atlantic forest fragmentation studies. It is
the best available contemporary scenario because Coimbra
is the largest remaining Atlantic forest patch in northeast
Brazil (Tabarelli et al., 2006), and its core areas of undisturbed
forest interior (sensu Harper et al., 2005) can be used as ‘con-
trol’ sites to assess the long-term effects of habitat fragmen-
tation on the structure of tree assemblages. We are aware,
however, 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,
unreplicated tract of forest at the landscape and regional
scales.
2.2. Tree inventories and habitat classification
Trees P10 cm in diameter at breast height (DBH) were inven-
toried in four habitat types: (1) Forest edge: peripheral areas
within 100 m of the border of the largest fragment (Coimbra
Forest). (2) Core area: old-growth forest interior areas of the
Coimbra Forest beyond 200 m of the border and showing no
detectable edge influence. Our definitions of forest edges
and core areas are based on Laurance et al. (2002), who
showed that most edge effects penetrate less than 200 m into
Amazonian forest fragments. (3) Forest gaps: small (<2 ha)
regenerating patches of secondary forests of known age lo-
cated within core areas of the Coimbra Forest. Secondary for-
est patches consisted of 5–65-yr-old chronosequences created
by the abandonment of slash-and-burn plots following 5–10
yrs of subsistence agriculture (maize, cassava, beans). The
age (yrs) of secondary stands were determined to within a
6-month error by comprehensive interviews with long-term
residents and company employees who had long been in
charge of subsistence agriculture at these sites. (4) Small for-
est fragments: 20 forest fragments ranging between 3.4 and
79.6 ha in size, and entirely surrounded by sugar-cane fields.
Location of all sites was recorded using a handheld GPS.
2.3. Functional attributes of tree assemblages
To characterize tree assemblages we sampled 75 plots of
0.1 ha (10 · 100 m) in each of the four habitats including: (1)
10 forest edge plots placed randomly along the 39.9-km
perimeter of the Coimbra Forest, starting at the forest edge,
252 B I O L O G I C A L C O N S E RVAT I O N
and penetrating perpendicularly 100 m into the fragment; (2)
20 core area or forest interior plots randomly placed at
>200 m from the Coimbra Forest edge; (3) 25 secondary forest
plots placed within 25 different secondary forest patches (one
plot per patch; Fig. 1) located in the Coimbra Forest; and (4)
one plot located at the geometric center of each of the 20
small forest fragments. We allocated a lower sampling effort
to forest edges (n = 10 plots) because this habitat is expected
to be taxonomically more homogeneous than core areas
and forest fragments (see Oliveira et al., 2004; Laurance
et al., 2006a). Between-plot distance across the four habitats
varied from 218 m up to 24,217 m, and the average distance
between all 75 plots exceeded 1000 m. Finally, the distance be-
tween tree plots and the nearest forest edge was 0 m for forest
edge plots, 200–757.6 m for forest interior plots, 31.8–578.3 m
for second-growth plots, and 72.4–248.5 m for plots in small
forest fragments.
All trees P10 cm DBH within each plot were measured and
identified to species level. Plant vouchers are available at the
Federal University of Pernambuco, UFP Herbarium, Brazil
(voucher Nos. 34,445–36,120). All tree species were assigned
to categories describing their regeneration strategy, vertical
stratification within each site, seed-dispersal mode and seed
size using: (1) a comprehensive literature review, including
books, papers, plant monographs, and MSc and PhD disserta-
tions (e.g. van Roosmalen, 1985; Lorenzi, 1998; Barroso et al.,
1999; Grillo, 2005; several issues of Flora Neotropica); (2) vou-
cher specimens housed in the eight major herbaria of north-
eastern Brazil; and (3) a fruit/seed collection (172 samples)
housed at the UFP Herbarium. These sources were further
supplemented by our own personal knowledge on 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).
Our functional groups of tree species are defined as follow-
ing: (a) regeneration strategy – shade-tolerant species are those
capable of regenerating in the shaded understorey of old-
growth forests; and pioneer species are those requiring high-
light environments provided by treefall gaps and forest edges
as viable regeneration sites (Hartshorn, 1978). This group also
included large or long-lived pioneer species (sensu Whitmore,
1989), the adults of which are usually found in the canopy or
emergent stratum of old-growth forests (Swaine and Hall,
1983); (b) forest stratification – understorey species consisted
of small trees and shrubs flowering and fruiting in the lowest
forest layer (<10 m); canopy species occurred in the forest
subcanopy and canopy; and emergent species occurred in the
highest forest layer (Wilson, 1989); (c) seed-dispersal mode –
vertebrate-dispersed species are those that produce diaspores
attached to a fleshy pulp, aril, or other features typically asso-
ciated with vertebrate dispersal agents; and abiotically-
dispersed species are those producing winged seeds, plumes,
or other wind-dispersal devices that slow the rate of seed fall
or those dispersed entirely by free fall or propelled explosively
by a fruit that opens suddenly, often triggered by a trip-lever
(van der Pijl, 1982); (d) Seed size of vertebrate-dispersed spe-
cies – small: 0.6–1.5 cm in length; and large: >1.5 cm in length.
All procedures, criteria, and categories used here to assign
tree species to functional groups have been used previously
1 4 1 ( 2 0 0 8 ) 2 4 9 –2 6 0
(Silva and Tabarelli, 2000; Tabarelli et al., 2003; Melo et al.,
2006).
Based on the above categories, scores for nine structural
and functional traits of tree assemblages (hereafter assem-
blage attributes) were calculated for each plot as following:
(1) stem density per plot; (2) tree species richness per plot;
and percentage of (3) pioneer species; (4) pioneer stems; (5)
emergent species; (6) canopy species; (7) understorey species;
(8) vertebrate-dispersed species; and (9) large-seeded species.
2.4. Explanatory variables
Because a number of patch and landscape-scale environmen-
tal variables may contribute to differences in the structure of
tree assemblages, we consider the effects of soil type, vegeta-
tion type, forest fragment size, distance to the nearest forest
edge, and the amount of forest cover retained in the sur-
rounding landscape, in addition to the spatial structure of for-
est plots sampled. Landscape-scale forest cover is positively
correlated with overall connectivity between patches (Gorre-
sen and Willig, 2004) and was quantified as the percentage
of forest within a 1-km external buffer set from the perimeter
of each fragment. Patch and landscape metrics were quanti-
fied 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 by the Usina Serra Grande Agriculture Office.
2.5. Data analysis
Differences between forest edge, forest interior, forest gap
and small fragment plots in the relative abundance of trees
sharing different functional traits were examined using the
following complementary approaches. First, between-habitat
differences were tested using one-way ANOVAs followed by
Tukey post hoc comparisons. Second, we used linear regres-
sion models to describe the relationship between the age of
second-growth stands within forest gaps and tree assemblage
attributes. Third, general linear models (GLMs) were used to
detect any effect of explanatory variables on tree assemblage
attributes by first examining the effects of habitat type, soil
type, vegetation type and distance to the nearest edge consid-
ering all 75 plots across the four habitats, and then the effects
of forest fragment size and surrounding forest cover on tree
assemblages in the 20 small fragments. Forest edge, second-
growth and forest interior plots were excluded from the latter
GLMs because they were unavoidably placed within the same
large fragment (Coimbra Forest). All plots were assigned into
two mutually exclusive vegetation types (evergreen and
semi-deciduous forest) and soil types (yellow-red latosol
and yellow-red podzol). Finally, we re-examined environmen-
tal effects on functional attributes of tree assemblages using
general linear mixed models (GLMM) to account for the po-
tential lack of spatial independence of tree plots within the
largest forest fragment. GLMMs were fitted to model different
habitat, patch and landscape variables which were entered as
fixed effects, whereas assemblage attributes were assumed to
be nested within clusters (fragments) over which the random
 B I O L O G I C A L C O N S E RVAT I O N 1 4 1 ( 2 0 0 8 ) 2 4 9 –2 6 0 253

effects varied. The R package (v. 2.2.0) was used to fit the
GLMMs using a logit link function. All response variables
(assemblage attributes) fitted a normal distribution (Lilliefors
tests: Sokal and Rohlf, 1995), but some of the explanatory
variables were transformed to stabilize variance, improve nor-
mality of data and consequently increase the explanatory
power of models (see Tables 3 and 4).
To test the hypothesis that forest edge and small fragment
plots were taxonomically more similar to those of second-
growth patches than those in the forest interior of the largest
fragment, we performed a non-metric multidimensional scal-
ing (NMDS) ordination of all 75 plots using their Bray–Curtis
dissimilarity matrix of species composition (Krebs, 1989). Spe-
cies abundance data were sqrt-transformed and standardized
(sensu Clarke and Gorley, 2001) in order to avoid any bias
resulting from highly abundant species and differences in
sample sizes (i.e. stem density per plot). To examine the rela-
tionships between habitat type, vegetation type and soil type
on the species similarity between plots, these variables were
considered as factors in ANOSIM tests (Clarke and Gorley,
2001). We also performed a Mantel test with weighted Spear-
man rank correlation to address the effect of plot location on
levels of taxonomic similarity. Straight-line distances be-
tween plots were ln-transformed, as suggested by Condit
et al. (2002) and Jones et al. (2006), and postulated by Hubbell’s
(2001) neutral theory. Finally, we performed an indicator spe-
cies analysis (sensu Dufrêne and Legendre, 1997) based on two
groups of tree plots identified by both NMDS ordinations and
ANOSIM tests: one consisting exclusively of forest interior
plots and another of forest edge, small fragment and sec-
ond-growth plots. All analyses were carried out using Systat
(Wilkinson, 1996), Primer (Clarke and Gorley, 2001) and PC-
Ord (McCune and Mefford, 1999).
3. Results
A total of 5398 live trees and 219 tree species were recorded in
the 75 plots (total area = 7.5 ha) inventoried. Tree assemblages
in forest edge, small forest fragment and second-growth plots
were significantly different from those in forest interior in
terms of seven of the nine assemblage attributes considered
(Table 1). Major differences included stem density, tree spe-
cies richness, proportion of pioneer stems and pioneer spe-
cies, and proportion of large-seeded species. Forest edges
exhibited the largest differences compared to forest interior
plots despite the fact that these two habitats were embedded
within the same large fragment (Coimbra Forest) and sepa-
rated by shorter distances; edge and forest interior plots were
on average 2480.4 m ± 960.2 m apart (n = 200 pairs). Compared
to forest interior sites, forest edges retained only half of the
total species richness but three times the richness and abun-
dance of pioneer species, amounting to a highly biased ratio
between pioneer and shade-tolerant species.
The age of second-growth stands explained between 31.4%
and 88.2% of the variation in tree assemblage attributes in this
habitat, and forest gap age correlated positively with most of
the attributes examined (Table 2). As expected, forest edge
and forest fragment plots exhibited tree assemblage attributes
within the range of values shown by either early (<25-yr old) or
mid-successional secondary forest plots (25–45-yr old),
whereas forest interior plots exhibited values more typical of
late-successional secondary forests (>45-yr old) or outside
their range (Fig. 2). This is consistent with the fact that forest
edges were more similar to early secondary forests in terms of
overall species richness, and abundance and species richness
of pioneer, emergent and large-seeded species. GLMs failed to
detect any significant effect of vegetation type and soil type on
any of the structural or functional attributes of tree assem-
blages across the four habitats. On the other hand, GLMs
clearly identified habitat type and distance to the nearest for-
est edge as the most significant explanatory variables driving
the changes in tree assemblage structure regardless of plot
location in the landscape. These two variables combined ex-
plained between 20.9% and 40.4% of the variation in tree
assemblages such as the proportion of emergent species,
large-seeded species and pioneer stems (Table 3). Other patch
and landscape metrics, such as forest fragment area and for-
est cover in the surrounding landscape, played a minor role.
This was supported by the GLMMs which consistently pin-
pointed distance to the nearest forest edge and age of forest
stands as the only significant explanatory variables for all
functional attributes of tree assemblages (Table 4).
NMDS ordination of tree plots based on species similar-
ity and abundance resulted in two consistent and clearly

Table 1 – Tree assemblage attributes (mean ± SD) in 0.1-ha plots located along forest edges and in small forest fragments,
secondary forest patches, and core forest interior at Usina Serra Grande, Brazil
Assemblage attributes Forest edge Small fragments Secondary forest Old-growth forest ANOVA
(n = 10) (n = 20) patches (n = 25) interior (n = 20)
F p
a a,b b c
Stem density (per 0.1 ha) 59.8 ± 7.5 73.8 ± 25.4 51.6 ± 18.5 101.6 ± 21.7 23.3 <0.0001
Total species richness 18.4 ± 4.5a 23.7 ± 9.6a 20.6 ± 9.8a 36.8 ± 7.3b 16.5 <0.0001
Pioneer species (%) 88.1 ± 7.5a,c 72.6 ± 13.3b 80.5 ± 14.4b,c 41.8 ± 12.7d 43.4 <0.0001
Pioneer stems (%) 93.8 ± 5.6a 78.9 ± 15.6b 85.6 ± 13.8a,b 37.7 ± 16.4c 54.6 <0.0001
Emergent species (%) 9.5 ± 5.5a 15.1 ± 8.7a 16.1 ± 8.1a 27.4 ± 4.8b 17.3 <0.0001
Canopy species (%) 79.6 ± 8.2a 75.6 ± 9.2a 78.1 ± 10.01a 63.2 ± 6.4b 13.6 <0.0001
Understorey species (%) 10.8 ± 6.7a 9.1 ± 4.4a,b 5.6 ± 4.6a,c 9.2 ± 4.5a 3.77 0.014
Vertebrate-dispersed species (%) 83.5 ± 4.2 78.4 ± 9.4 83.3 ± 11.04 83.2 ± 13.9 0.98 0.400
Large-seeded species (%) 9.4 ± 8.1a 27.6 ± 9.7b 20.5 ± 15.01a,b 49.4 ± 11.3c 32.3 <0.0001

Significant differences in post hoc comparisons (Tukey tests) between habitat types are indicated by different letters in a same row, where
effects were significant within analysis of variance. Values in bold denote significant differences.
254 B I O L O G I C A L C O N S E RVAT I O N 1 4 1 ( 2 0 0 8 ) 2 4 9 –2 6 0

Table 2 – Tree assemblage attributes and linear regression equations describing their variation within 25 second-growth
plots placed in 25 spatially independent patches of 5–65-yr-old secondary forest at Usina Serra Grande, northeastern
Brazil
Assemblage attributes Equations R2 (%) F p
a
Stem density (ha) y = 18.768 + 1.015x 69.6 52.6 <0.0001
Total species richness y = 3.293 + 0.537x 88.2 51.03 <0.0001
Pioneer species (%) y = 99.88  0.599x 41.3 15.07 0.001
Pioneer stems (%) y = 106.44  0.643x 50.3 23.28 <0.0001
Emergent species (%) y = 5.226 + 0.339x 47.0 15.02 0.001
Canopy species (%) y = 92.5  0.443x 45.3 19.05 <0.0001
Understorey species (%) y = 2.12 + 0.104x 11.7 3.04 0.094
Vertebrate-dispersed species (%) y = 90.56  0.224x 0.09 2.41 0.134
Large-seeded species (%) y = 2.841 + 0.547x 31.4 10.21 0.004

Values in bold denote significant effects.

a Age of secondary forest patches in years.

Fig. 2 – Relationships between time of recovery (age, yrs) of 25 secondary forest patches within the Coimbra Forest (forest gap)
and the (a) total number of tree species, (b) percentage of large-seeded species, (c) percentage of pioneer species, and (d)
percentage of emergent species at Serra Grande, Brazil. R2-values are shown for each relationship. The mean (solid line),
median (thin line), 25th and 75th percentiles (boundaries of boxes), and 5th and 95th percentiles (whiskers above and below
box plots) are also indicated for each of these functional attributes for equal-sized plots within (F) small forest fragments, (E)
forest edges and (C) core areas of old-growth forest interior.

segregated clusters: one formed by the 20 forest interior, old-
growth plots and another formed by the forest edge, small
fragment and second-growth plots (Fig. 3a and b). Plot ordina-
tion was well supported by low stress levels of 0.16 and 0.13.
In addition, ANOSIM uncovered no significant correlation be-
tween soil type and degree of taxonomic similarity between
plots (R = 0.092; p = 0.995), but detected a small effect of vege-
tation type (R = 0.26; p = 0.006) and a stronger effect of habitat
type (R = 0.54; p = 0.001). Tree community structure in forest
interior plots was significantly different from that along edge
(R = 0.934; p = 0.001) and second-growth plots (R = 0.79;
p = 0.001) within the large remnant, despite their relative spa-
tial proximity. Forest interior plots were also significantly dif-
ferent from those in small fragment (R = 0.79; p = 0.001). This
 B I O L O G I C A L C O N S E RVAT I O N 1 4 1 ( 2 0 0 8 ) 2 4 9 –2 6 0 255

Table 3 – Results from generalized linear models applied to five tree assemblage attributes in all four forest habitats (n = 75
plots) at Serra Grande, northeastern Brazil

Assemblage attributes Explanatory variables (p-values)

Habitat type Vegetation type Soil type Distance to edge (log10 x + 1) Whole model R2 (%)

Species richness 0.037 0.519 0.75 0.028 <0.0001 20.9

Pioneer species (%) 0.002 0.598 0.80 0.046 <0.0001 27.3
Emergent species (%) 0.017 0.13 0.66 <0.0001 <0.0001 40.4
Large-seeded species (%) 0.021 0.39 0.67 0.020 <0.0001 23.7
Pioneer stems (%) 0.0001 0.43 0.78 0.042 <0.0001 33.1

Table 4 – Results from generalized linear mixed models (GLMMs) examining five tree assemblage attributes across four
different forest habitats at Serra Grande, northeastern Brazil
Assemblage attributes Explanatory variables Estimate (±SE) DF t-Ratio p-Value

Species richness Forest fragment 0.95 (0.36) 17 2.63 0.017

Fragment area (log10 ha) 0.97 (2.89) 17 0.33 0.742
Distance to nearest edge (log10 m) 12.52 (2.45) 52 5.12 <0.0001
Surrounding forest cover 0.05 (0.26) 17 0.18 0.858
Age of stand (sqrt yrs) 1.97 (0.29) 52 6.57 <0.0001

Pioneer species (%) Forest fragment 1.21 (0.76) 17 1.59 0.129

Fragment area (log10 ha) 1.15 (4.6) 17 0.23 0.814
Distance to nearest edge (log10 m)  31.6 (5.6) 52 5.57 <0.0001
Surrounding forest cover 0.35 (0.56) 17 0.63 0.537
Age of stand (sqrt yrs) 4.8 (0.69) 52 6.8 <0.0001

Shade-tolerant species (%) Forest fragment 1.11 (0.66) 17 1.68 0.112

Fragment area (log10 ha) 0.48 (4.07) 17 0.12 0.906
Distance to nearest edge (log10 m) 25.84 (4.93) 52 5.24 <0.0001
Surrounding forest cover 0.067 (0.49) 17 0.14 0.892
Age of stand (sqrt yrs) 3.89 (0.61) 52 6.40 <0.0001

Emergent species (%) Forest fragment 0.47 (0.29) 17 1.6 0.123

Fragment area (log10 ha) 0.64 (1.9) 17 0.34 0.736
Distance to nearest edge (log10 m) 14.8 (1.8) 52 7.9 <0.0001
Surrounding forest cover 0.42 (0.21) 17 1.9 0.063
Age of stand (sqrt yrs) 1.19 (0.22) 52 5.2 <0.0001

Large-seeded species (%) Forest fragment 0.82 (0.59) 17 1.36 0.189

Fragment area (log10 ha) 1.99 (3.6) 17 0.53 0.597
Distance to nearest edge (log10 m) 22.7 (4.4) 52 5.06 <0.0001
Surrounding forest cover 0.13 (0.44) 17 0.29 0.77
Age of stand (sqrt yrs) 2.79 (0.55) 52 5.06 <0.0001

Fig. 3 – NMDS ordination of 75 plots based on Bray–Curtis species similarity coefficients: (a) 75 plots within all four habitats;
and (b) 55 plots located within the Coimbra Forest only. Triangles, open squares, open circles and dark shaded circles
represent plots in small forest fragments (n = 20), forest edges (n = 10), second-growth patches (n = 25), and core areas of
primary forest (n = 20).
256 B I O L O G I C A L C O N S E RVAT I O N 1 4 1 ( 2 0 0 8 ) 2 4 9 –2 6 0

Table 5 – Indicator species analysis (sensu Dufrêne and Legendre, 1997) of tree assemblages recorded in forest edge, small
fragment, and second-growth plots (Group 1); and forest interior plots (Group 2) at Serra Grande, northeastern Brazil

Indicator species Family Regeneration strategy Group Indicator value (IV) IV randomized groups p

Tapirira guianensis Anacardiaceae Pioneer 1 82.3 49.4 ± 6.8 0.001

Byrsonima sericea Malpighiaceae Pioneer 1 75.0 41.3 ± 7.5 0.002
Bowdichia virgilioides Fabaceae Pioneer 1 68.7 38.7 ± 7.74 0.003
Schefflera morototoni Araliaceae Pioneer 1 60.9 34.7 ± 7.1 0.006
Ocotea glomerata Lauraceae Pioneer 1 60.9 35.2 ± 7.5 0.007
Brosimum rubescens Moraceae Pioneer 1 56.2 32.7 ± 7.41 0.014
Thyrsodium spruceanum Anacardiaceae Pioneer 1 53.6 34.5 ± 7.8 0.027
Himatanthus bracteatus Apocynaceae Pioneer 1 40.6 26.4 ± 7.3 0.046
Mabea occidentalis Euphorbiaceae s-Tolerant 2 94.6 20.6 ± 6.6 0.001
Virola gardneri Myristicaceae s-Tolerant 2 95.5 17.5 ± 6.2 0.001
Licania belemii Chrysobalanaceae s-Tolerant 2 82.6 17 ± 6.1 0.001
Sloanea obtusifolia Elaeocarpaceae s-Tolerant 2 77.6 12.9 ± 5.5 0.001
Helicostylis tomentosa Moraceae s-Tolerant 2 74 15.6 ± 5.6 0.001
Inga edulis Fabaceae Pioneer 2 72.2 17 ± 6.1 0.001
Tovomita mangle Clusiaceae s-Tolerant 2 69.6 11 ± 4.7 0.001
Pterocarpus violaceus Fabaceae Pioneer 2 63.4 16.6 ± 6.6 0.001

Key indicator species (only eight species with the highest indicator values (IV) are listed for each group) show their regeneration strategy and IV.

was confirmed by a Mantel test which failed to uncover any
large-scale spatial effect on the taxonomic similarity across
all 75 plots (q = 0.155; p = 0.95). Finally, the indicator species
analysis underscored the occurrence of eight indicator spe-
cies (all of which pioneers) in the floristically cohesive group
of plots formed by forest edges, small fragments and second-
ary forest patches (Group 1). In contrast, 32 indicator species
of shade-tolerant trees (from a set of 41 indicator species)
were evident in the samples of forest interior plots (Group 2,
Table 5). This clearly indicates that the taxonomic segregation
between primary, secondary and edge-affected forest habitats
was driven by the occurrence and relative abundance of spe-
cies within different functional groups.
4. Discussion
4.1. Patterns and underlying mechanisms
This study shows highly predictable patterns of tree commu-
nity drift in Atlantic forest fragments that have experienced a
long but stable history of relaxation over at least 60 years of
isolation. Further, tree communities subjected to a post-isola-
tion history of forest disturbance resulting from either edge
effects or clear-cutting showed a large degree of functional
convergence that cannot be explained by soil types, vegeta-
tion types, or the spatial position of the plots sampled. Other
neotropical studies have shown that tree assemblages along
forest edges and in small fragments (1–10 ha) become rapidly
and increasingly more impoverished, dominated by a small
set of pioneer species, and are poorly represented in terms
of several ecological groups of trees occurring in undisturbed
primary forest, such as emergent and large-seeded species
(BDFF project: Laurance, 1997, 2001; Laurance et al., 2006b).
However, the full extent of this floristic simplification process
remains poorly understood as the small fragments experi-
mentally created in the BDFF study of central Amazonia,
north of Manaus, have not yet achieved relaxation in their
25-yr post-isolation history (see Laurance et al., 2006a). Time
lags in plant assemblage responses to changes in habitat con-
figuration may be far more prolonged (Lindborg and Eriksson,
2004), particularly for long-lived trees. Additionally, some ef-
fects on forest dynamics resulting from sudden habitat reduc-
tion and isolation are expected to become less pronounced
with time (Kapos et al., 1997; Sizer and Tanner, 1999).
Our results indicate that tree assemblages in small frag-
ments and along the edges of the largest remaining forest
remnant of northeast Brazil are much more similar to those
in early- to mid-successional secondary forest stands than
to core old-growth forest patches showing no detectable edge
influence. Both forest edges along a very large remnant and
core areas of small fragments retained only half of the total
tree species richness, and less than one-third of the shade-
tolerant, emergent, and large-seeded tree species found in
primary forest interior plots. Conversely, the total number of
pioneer stems and pioneer species increased at least fourfold
in forest-edge and small fragment plots compared to those in
forest interior conditions. Furthermore, forest plots domi-
nated by edge effects shared the same set of indicator pioneer
species, irrespectively of the fragment in which they had been
placed and their location in the landscape. This implies that
forest fragment archipelagos in old deforestation frontiers
that are overwhelmingly dominated by small forest patches,
as it is typically the case throughout the humid tropics (Ranta
et al., 1998; Gascon et al., 2000), may be comprised of no more
than a collection of early- to mid-successional secondary for-
est stands in terms of their tree life history traits. Should this
be true, many floristic trends documented in more recently
fragmented forest landscapes, such as those in central (Lau-
rance, 2001) and southern Amazonia (Michalski et al., 2007),
represent but the first steps towards a more drastic and per-
vasive simplification of tree assemblages. Although our study
has failed to monitor forest composition over many decades
of isolation, it provides what is to our knowledge the first
set of reliable indicators of the long-term transitions in tree
functional groups in a fragmented neotropical forest land-
scape and gives support to the notion that severely frag-
 B I O L O G I C A L C O N S E RVAT I O N
mented landscapes tend to retain non-random nested-sub-
sets of species from the original source flora as postulated
by Patterson (1987).
Although a dozen or so studies have documented that, at
both regional and landscape scales, the distribution and
abundance of several tropical tree species may be affected
by soil type (e.g. Clark et al., 1998; ter Steege et al., 2006),
edaphic conditions apparently played only a minor role in
the patterns describe here. In fact, there is no empirical sup-
port for the notion that, at the landscape scale, variation in
the relative contribution of tree functional groups in undis-
turbed neotropical terra firme forests can be attributed to var-
iation in soil properties, whether these are coarsely quantified
using regional scale soil maps, or based on soil samples col-
lected at each forest plot. Instead, changes in tree assemblage
structure documented here are largely explained by rather
predictable declines or increases in the relative contribution
of species sharing similar life-history traits, such as seed size,
dispersal mode and regeneration strategy. Edge effects and
synergistic processes that may operate concurrently with for-
est fragmentation are still the most powerful forces driving
changes in both the taxonomic and functional composition
of tree assemblages stranded in tropical forest fragments
(Tabarelli et al., 2004; Michalski et al., 2007).
Changes in the functional attributes of tree assemblages
described here probably resulted from a myriad of biotic
and abiotic processes that can either favour the establish-
ment and spread of pioneer species, or suppress the recruit-
ment of shade-tolerant and mature forest species, which
may eventually result in their local to regional-scale extirpa-
tion. One common feature among most of these processes
is that they result from forest-edge creation and the influence
of the surrounding matrix, rather than erosion of connectivity
or habitat loss per se (Laurance et al., 2002; Tabarelli and Gas-
con, 2005). For example, proliferation of pioneers following
the creation of forest edges is fueled by elevated rates of tree-
fall gaps and the collapse of the emergent stratum (Laurance
et al., 1998, 2006a). Peripheral treefall gaps and edge-related
microclimatic changes then further promote suitable condi-
tions for a striking recruitment and growth of pioneers within
100 m of fragment margins (Laurance et al., 2002, 2006a).
It has been postulated that forest fragmentation and the
ensuing creation of forest edges can gradually deplete popula-
tions of shade-tolerant trees in small fragments and near
edges of large fragments through a myriad of processes
affecting most stages of the plant life cycle (e.g. Tabarelli
et al., 2004). Potentially, population collapse in edge-sensitive
forest interior species can be caused by: (1) reduced seed flux
(Benı́tez-Malvido and Martı́nez-Ramos, 2003); (2) increased
seedling mortality caused by litterfall suppression, patho-
gens, increased herbivory and treefall damage near forest
edges (Benı́tez-Malvido, 1998; Didham and Lawton, 1999;
Benı́tez-Malvido and Lemus-Albor, 2005; Wirth et al., 2007);
(3) increased sapling/adult mortality resulting from competi-
tion with lianas, vines and ruderal species (Pérez-Salicrup,
2001); and (4) increased adult mortality caused by physiologi-
cal stress from desiccation and wind turbulence resulting in
elevated rates of both uprooting and breakage (D’Angelo
et al., 2004). Furthermore, edge habitat can drastically affect
seed shadows for different plant functional groups. For exam-
1 4 1 ( 2 0 0 8 ) 2 4 9 –2 6 0 257
ple, the seed rain within old edges along the perimeter of the
Coimbra Forest – the 35-km2 remnant surveyed here – is
markedly reduced for large-seeded tree species (Melo et al.,
2006). Low rates of seed delivery may therefore be an addi-
tional force reducing the establishment of large-seeded trees
in forest edges of large patches or anywhere in small patches
(Chapman et al., 2003; Melo et al., 2007).
4.2. Forest regeneration vs. degeneration
Although tree assemblages in edge-dominated habitats had
properties similar to those of secondary forest patches sur-
rounded by large areas of old growth, this does not imply that
edges and small fragments can support regenerating forests at
the patch scale. Briefly, forest regeneration, or secondary for-
est succession, consists of a forest recovery process following
severe perturbation events, which can either be natural (e.g.
large treefall gaps) or anthropogenic (e.g. forest conversion
for slash-and-burn agriculture) (Brown and Lugo, 1990; Tabar-
elli and Mantovani, 2000). In the case of secondary forest
patches considered here, which resulted from slash-and-burn
agriculture based on clear-cutting of small patches of old-
growth forest, forest regeneration is expected to occur through
a directional sequence of establishment and replacement of
seral stages, from the initial colonization stage consisting of
weedy or scrub-dominated communities to tree-dominated
communities as described by Richards (1996). Along these ser-
al stages, pioneer plants are replaced by shade-tolerant trees
and the tree assemblage gradually accumulates biomass and
becomes increasingly more diverse in both taxonomic and
ecological terms (i.e. higher diversity of plant life-history traits
irrespective of their taxonomic composition; Richards, 1996;
Guariguata and Ostertag, 2001).
At the patch scale, however, plant assemblages in small
forest patches and edges of large patches appear to face an in-
verse process as more complex, high-diversity assemblages
dominated by shade-tolerant trees typical of old-growth for-
ests (e.g. large-seeded, emergent and hardwood tree species)
become impoverished through the gradual replacement of
these species by a small dominant set of persistent, fast-
growing pioneer species that accrue a low biomass due to
their smaller size and low wood density (Chave et al., 2006).
In sum, we hypothesize that creation of forest edges triggers
a forest degeneration process, or a retrogressive succession at
the habitat patch scale in which plant communities will re-
tain gradually fewer species and lower biomass over time.
In small fragments and edge-dominated areas of even the
largest fragments this degeneration process is driven by a
combination of mechanisms that: (i) facilitate the recruit-
ment and growth of pioneers, and (ii) deplete populations of
shade-tolerant trees, which represent the dominant regener-
ation guild in tropical primary forests (Whitmore, 1991). In the
long run, theses habitats will tend to retain an increasingly
simplified (degenerated) tree assemblage, which just so hap-
pens to converge (following an inverse species turnover tra-
jectory) with those of regenerating stands in small
secondary forest patches that can still benefit from the input
of surrounding areas of old-growth forest.
Given current primary forest conversion rates, it appears
inevitable that tropical forests will be transformed into
258 B I O L O G I C A L C O N S E RVAT I O N
human-dominated landscapes, with pervasive consequences
for the long-term persistence of biodiversity (Corlett, 2000;
Peres, 2001; Wright and Muller-Landau, 2006). For example,
the Brazilian government intends to massively expand biofuel
production from sugarcane ethanol, which poses an addi-
tional threat to the already severely fragmented Atlantic for-
est biome. To offset these trends, large efforts have been
allocated to formulate landscape management guidelines,
which are assumed to reduce the probability of biodiversity
loss (see Bierregaard et al., 2001; Tabarelli and Gascon, 2005).
The most appealing modern set of guidelines refers to the
concept of biodiversity corridor – a network of protected areas
that are connected by relatively narrow forest corridors im-
mersed in a benign landscape where land use can coexist
with biodiversity (Sanderson et al., 2003). Such networks have
come to represent the basic foundation of any effective biodi-
versity conservation strategy in highly fragmented biomes. In
the Atlantic forest region of eastern and southeastern Brazil,
for instance, restoring corridor connectivity has been advo-
cated as the ultimate strategy to avoid massive species loss
(Silva and Tabarelli, 2000; Galindo-Leal and Câmara, 2003;
Tabarelli et al., 2005). Our results suggest that conservation
planning guidelines, such as creation and/or maintenance
of biodiversity corridors, will in fact fail to protect fragmented
forest landscapes from drastic species loss if the remnant (or
recreated) tracts of forests consist primarily of edge habitat.
At the landscape scale, biodiversity conservation could be im-
proved by retaining a significant amount of core forest habi-
tat, by gradually improving the shape and augmenting the
size of forest fragments, and by alleviating matrix harshness.
Acknowledgments
This study was made possible by research grants from CNPq
(to M. Tabarelli), Fundação O Boticário de Proteção à Natureza,
and Conservation International – Brasil. W.F. Laurance and
two anonymous reviewers offered constructive criticisms on
manuscript.
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