Landscape Ecol (2012) 27:799812
DOI 10.1007/s10980-012-9729-0
RESEARCH ARTICLE
How deforestation pattern in the Amazon influences
vertebrate richness and community composition
Paula Ribeiro Prist Fernanda Michalski
Jean Paul Metzger
Received: 3 June 2011 / Accepted: 20 February 2012 / Published online: 4 March 2012
Springer Science+Business Media B.V. 2012
Abstract The effects of habitat configuration on
species persistence are predicted to be most apparent
when remaining habitat cover is below 30%. We tested
this prediction by comparing vertebrate communities in
21 landscapes located in the southern Amazonia, includ-
ing 7 control landscapes (*100% of forest cover) and 14
fragmented landscapes (4 9 4 km). The fragmented
landscapes retained similar proportions of forest
(*25%), but had contrasting configurations, resulting
from two different deforestation patterns: the fish-bone
pattern common in small properties, and the large-
property pattern generally used by large ranchers.
Vertebrates were surveyed in all landscapes in Febru-
aryJuly 2009 with interviews (n = 150). We found a
significant difference in reported species richness
Electronic supplementary material The online version of
this article (doi:10.1007/s10980-012-9729-0) contains
supplementary material, which is available to authorized users.
P. R. Prist (&)  J. P. Metzger
Department of Ecology, Bioscience Institute, University
of Sao Paulo, Rua do Matao, 321, Travessa 14, Sao Paulo,
SP 05508-900, Brazil
e-mail: pprist@hotmail.com
F. Michalski
Postgraduate Programme in Tropical Biodiversity, Federal
University of Amapa, Rod. Juscelino Kubitschek, km 02,
Macapa, AP 68902-280, Brazil
F. Michalski
Pro-Carnvoros Institute, Av. Horacio Neto, 1030,
Atibaia, SP 12945-010, Brazil
among the fish-bone, large-property, and control areas
(mean = 29.3, 38.8 and 43.5 respectively). Control areas
and large-properties tended to have a higher number of
specialist species (mean = 13.7, and 11.7, respectively),
when compared with the fish-bone pattern (5.1). Verte-
brate community composition in the control and large-
properties was more similar to one another than to those
of the fish-bone landscapes. The number of fragments
was the main factor affecting the persistence of species,
being negatively associated with specialist species rich-
ness. Species richness was also positively related with the
size of the largest fragment structurally connected to the
studied landscapes (i.e., a regional scale effect). Our
results demonstrated that the large-property pattern,
which results in less fragmented landscapes, can maintain
a more diverse community of large vertebrates, including
top predators, which are considered fundamental for
maintaining ecosystem integrity. These results support
the hypothesis that landscape configuration contributes to
the persistence and/or extirpation of species.
Keywords Large vertebrates  Deforestation
patterns  Landscape ecology  Landscape
configuration  Species persistence  Brazilian Amazon
Introduction
Habitat loss and fragmentation have been the two main
consequences of the intense human pressure experi-
enced in the tropics in recent decades (Bernard and
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Fenton 2007). They both cause isolation of remnant
forest patches, thereby increasing risks of extinction
(Bodmer et al. 1997; Laurance et al. 2011) and
reducing native species richness (Stratford and Stouf-
fer 1999; Cullen et al. 2000; Ferraz et al. 2007).
Fragmentation can be understood as a modification in
the spatial arrangement of habitat patches, where a
large expanse of habitat is transformed into smaller
patches, resulting in many different spatial patterns
(Fahrig 2003). Habitat fragmentation reflects one
aspect of habitat configuration, and fragmentation
effects are distinct from habitat loss (Swift and
Hannon 2010).
Despite an extensive literature showing the impor-
tance of patch area and habitat loss to predict the
persistence of species, there are few studies discussing
the consequences of habitat configuration for main-
taining biodiversity in fragmented landscapes. Accord-
ing to the literature and previous empirical studies, it is
expected that population size should be related to
habitat loss in landscapes with a high proportion
([30%) of habitat, while in landscapes below this
threshold, the configuration of habitat patches should
more intensively influence species richness and/or
population size (Andren 1994; Fahrig 1998). As a
consequence, habitat configuration is expected to be
more important for population persistence in land-
scapes in which small amounts of the original habitat
remain (Fahrig 1998). In this situation one should ask
the following question: which habitat configuration is
more suitable to maintain biodiversity?
Studies of landscapes resulting from different
deforestation patterns are necessary to understand
the influences of habitat configuration on patterns of
species persistence and community dynamics. Defor-
estation patterns can be defined according to the size
and spatial distribution of deforested areas (Oliveira-
Filho and Metzger 2006). In the Brazilian Amazon,
two different patterns can be easily identified, the
fish-bone pattern and the large-property pattern not completely understood.
(Oliveira-Filho and Metzger 2006). The fish-bone
pattern is common to small properties (usually 50 ha
in the Alta Floresta regionOliveira-Filho and Metz-
ger 2006), which have been regularly distributed along
roads. Such small properties were donated to small
farmers (Ferraz et al. 2005) by the Brazilian Govern-
ment colonization program in the 1970s (Metzger
2001). These small family farmers gradually erode
the remaining forest on their properties, deforesting
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Landscape Ecol (2012) 27:799812
ca. 23 ha per year (Fujisaka et al. 1996). In contrast,
the large-property pattern is characterized by rapid
deforestation over large areas ([1,000 ha), and is
primarily caused by livestock farmers (Ferraz et al.
2005; Michalski et al. 2008). Both patterns cause
fragmentation and habitat loss, but the remaining
habitat patches have different configurations and
temporal dynamics. The fish-bone pattern usually
results in forest remnants that are smaller, more
irregular and less connected when compared to the
large-property pattern (Oliveira-Filho and Metzger
2006).
The Amazon forest is one of the most extensive
tropical forests of the world (Ferraz et al. 2005), and
deforestation, fragmentation and degradation of hab-
itat pose major threats to Amazon biodiversity (Lau-
rance et al. 2002; Peres et al. 2010). Mammals are
among the most threatened species, being particularly
sensitive to habitat loss and fragmentation (Linden-
mayer et al. 2000). Birds are another vertebrate group
that are good indicators of disturbance in tropical
forests, responding to changes in local vegetation
structure and landscape scale processes, as well as
having an important role in forest regeneration (Bar-
low and Peres 2006).
Previous studies revealed negative effects of loss
and/or isolation of Amazonian forest remnants on the
species richness of medium-sized and large-bodied
vertebrates (Stratford and Stouffer 1999; Laurance
et al. 2002; Lees and Peres 2006; Michalski and Peres
2007). However, while some species for example
larger bodied carnivores and primates (Michalski and
Peres 2005; Michalski et al. 2006), are lost from small
and isolated habitat patches due to low densities, large
spatial requirements, and conflicts with humans, other
species may persist in relatively small forest patches
(Lees and Peres 2006; Michalski and Peres 2007). The
responses of medium-sized and large-bodied verte-
brates to habitat disturbance and deforestation are thus
In this study we examined how the structural
differences between two contrasting deforestation
patterns (fish-bone and large-property) in the Brazilian
Amazon affected the community composition and
richness of medium-sized and large-bodied verte-
brates. The studied landscapes had proportions of
remaining forest habitat (ca. 25%) just below the
threshold where configuration effects should be more
apparent. We used multi-model inference to identify
Landscape Ecol (2012) 27:799812
relationships between the landscape structure and
vertebrate species richness to understand the relative
importance of landscape components for maintaining
vertebrate diversity. Specifically, we linked interview
data with forest patch metrics to test the hypotheses
that (1) the fish-bone pattern retains a smaller number
of total and specialist species and (2) the fish-bone
pattern has a more negative effect on the community
composition of large vertebrate community.
Materials and methods
Study area and sampling design
This study was conducted in the region of Alta
Floresta (09530 S, 56280 W), in the southern Brazil-
ian Amazon (Fig. 1). The region is located in the
center of the Arc of Deforestation, the contempo- properties in Brazilian Amazonia (independent of
rary epicenter of Amazon deforestation (Costa and
Pires 2010). Alta Floresta has been subjected to high
deforestation rates since the early 1980s (Michalski
et al. 2008), resulting in a fragmented landscape
containing forest patches of varying size, shape, and
degree of connectivity surrounded by a matrix of
managed cattle pasture (Oliveira-Filho and Metzger
2006), which is the dominant historic and present day
land-use in Alta Floresta (Michalski et al. 2008, 2010).
The annual average precipitation and temperature is
2,350 mm and 24.5C, respectively, with high relative
humidity (8085%; RADAM BRASIL 1983). Alti-
tudes vary between 200 and 300 m. There is no
evidence to suggest that differences in forest cover
between landscapes are due to abiotic conditions and
as recently as 1976, the Alta Floresta region was
entirely covered by undisturbed Amazonian forest of
similar physiognomy (Oliveira-Filho and Metzger
2006; Michalski et al. 2007). Therefore, we assume
that there is no variation in forest type and composition
across the landscapes. This assumption is supported by
the fact that present day forest cover comprises
primarily mature forests, as in this region there is
little secondary forest regeneration due to intensive
cattle grazing (Michalski et al. 2008).
Twenty-one 4 9 4 km (1,600 ha) landscapes
were selected through the analysis of a georeferenced
2008 Landsat TM image (scene 227/67) (Fig. 1). The
study landscapes comprised seven fish-bone pattern,
seven large-property pattern and seven control areas
801
(continuous forest with [1,600 ha). Fish-bone and
large-property landscapes were selected based on a
visual inspection of the Landsat image (identified by
their characteristic deforestation patterns, Oliveira-
Filho and Metzger 2006) with approximately 25% of
forest cover (calculated from the classified image in
ArcGIS version 9.2; ESRI 19992006). All grids were
positioned within a regional context of similar forest
cover patterns such that we avoided possible con-
founding effects of differences in bordering habitat
configurations. Access by paved and unpaved roads,
and permission provided by landowners (all land-
scapes were formed by private properties) were the
final criteria for the selection of the landscapes.
All the landscapes selected were composed of
private properties that varied in size, but experienced
the same type of land use: cattle ranching. Brazilian
law (the Brazilian Forest Act) requires that all private
size) should maintain 80% of the native vegetation of
the property as legal reserve (Codigo Florestal 2001).
However, there is no concern about connectivity and
these legal reserves do not follow any pre-deter-
mined spatial plan. Despite this legal requirement,
only a minority of private properties respects this law.
Michalski et al. (2010) showed that from 300
landholdings surveyed in the Alta Floresta region,
only 20.3% still retained 80% or more of the property
area as native forest cover.
Vertebrate surveys
Obtaining species occurrence data through local
interviews is an effective approach that has been
successfully tested with medium-sized and large-
bodied vertebrates (Lawes et al. 2000; Michalski and
Peres 2005; Urquiza-Haas et al. 2009; Sampaio et al.
2010). To estimate vertebrate species richness in the
21 landscapes we conducted 150 interviews with local
landowners between February and July 2009 (fish-
bone: mean SD = 8 3, range = 515; large-
property: 7 3, range = 512; control landscapes:
5 1, range = 58, interviews). Focal species were
restricted to medium-sized and large-bodied mammals
([400 g) and birds ([200 g) that could be easily
identified by landowners. In our study area, each
of the fish-bone landscapes (4 9 4 km) encompassed
approximately 40 properties, while the large-property
landscapes and control areas usually included less
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Fig. 1 The region of Alta Floresta with the 21 landscapes
sampled in this study. The dark grey, light grey and black areas
represent forest, non-forest, and open water, respectively in a
than 10 properties. Therefore, we interviewed a
random sample of landowners in the fish-bone land-
scapes, while (almost) all landowners or land-manag-
ers (when landowners did not live in the region) were
interviewed in the other landscape types.
To ensure that we obtained reliable answers all
interviews were conducted with the assistance of a
local resident, known in the community. As a
prerequisite, interviewees were interviewed only if:
(1) they were willing to be interviewed, (2) had
knowledge of the fauna of the region, and (3) had lived
in or near the property for at least 2 years. In all cases
the interviews were accompanied by color plates with
images (photos and drawings) of all species known to
exist in the region (Michalski and Peres 2005, 2007;
Peres and Michalski 2006). To assess the frequency of
type II errors, we included seven species known to be
entirely absent from the study region. From the total of
150 interviews, we detected false-positive records in
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Landscape Ecol (2012) 27:799812
2009 Landsat TM image. The fish-bone landscapes 14 are
isolated, whereas units 57 are still structurally connected with
the surrounding forest
only two (1.33%) interviews (which we retained in our
analysis) suggesting a high level of reliability in our
results. All species were reported only if they were
present in the landscapes during the 5 years preceding
interviews, and a species was considered present only
when 50% or more of the interviews reported it as
present in the same landscape unit. This method does
not enable us to distinguish between resident or
transient species, thus we considered both as present in
the studied landscapes.
Within-patch disturbance and forest-patch metrics
Fragmentation and deforestation are commonly asso-
ciated with many synergistic disturbances that can
transform fragments into entirely new ecosystems
(Laurance et al. 2002, 2011; Peres and Michalski
2006; Peres et al. 2010). To characterize the intensity
and extent of disturbance within each landscape unit
Landscape Ecol (2012) 27:799812
we used information obtained from the local land-
owner interviews. Logging intensity and burn severity
were classified using a five-point scale: (0) none, (1)
light, (2) moderate, (3) heavy, and (4) very heavy. Our
measure of logging intensity took into account the
method of timber extraction, selection of tree species,
the relative amount of harvested timber, and the
number of years since the extraction stopped. Burn
severity (using the same five-point scale as above)
considered the proportion of forest that was burned
(edge or interior), and the number of fire occurrences
(Michalski and Peres 2005). We also derived a
qualitative hunting intensity index that included
information about the hunting history (frequency and
time since the last hunting event was recorded), the
hunting pressure (none, light, heavy), and if hunting
activities still took place when we conducted inter-
views (see supplementary online material for more
details).
Landscape variables were extracted from a Landsat
image (July 28th, 2009) using Fragstats (version 3.3;
McGarigal and Marks 1995) and ArcGIS (version 9.2;
ESRI 19992006). We applied an unsupervised clas-
sification to derive three land cover classes (forest,
non-forest and water), and assessed the accuracy of the
classified land cover map by comparing the 2009
classified image with 234 reference points obtained in
the field from February to July of 2009. This resulted
in 100% matching.
For each studied landscape we measured forest
proportion, number of fragments, and two temporal
variables: isolation age and deforestation age. These
temporal variables were measured from 14 biannual
Landsat-5 TM images (scene 227/67) dated from 1984
to 2009. The isolation age was defined as the number
of years since the studied landscape lost its structural
connectivity, i.e., when a forest patch does not span (or
percolate) the entire extent of the landscape (Stauffer
1985). Deforestation age was defined as the number of
years since the first event of deforestation could be
detected in the landscape unit from the Landsat scene.
All images used to derive these temporal variables
were aligned and georeferenced using the 2008
Landsat image as a base. We used at least 19 points
to align the images, resulting in a positional error of
less than one pixel (mean SD = 25.40 2.64 m).
To consider the landscape context at a broader
(regional) spatial scale, we also measured the size of
the largest forest area that was structurally connected
803
to the fragments inside the 4 9 4 km studied land-
scapes (hereafter referred to as largest connected
patch).
Data analysis
Total species richness and the richness of generalist
and specialist species were considered as response
variables and modeled separately in all further anal-
yses. The classification of vertebrates into generalist
(including: howler monkey, Alouatta seniculus; tayra,
Eira barbara; paca, Cuniculus paca) and specialist
species (including: red brocked deer, Mazama amer-
icana; white-lipped peccary, Tayassu pecari; jaguar,
Panthera onca) was based on forest dependence and
characteristics such as hunter preferences that were
obtained from an extensive literature review (see the
complete species classification list in Supplementary
Table S1).
We constructed curves of mean species richness
incremented by the interview sampling effort, with the
software EstimateS (Colwell 2005; version 7.5), to test
whether species richness had reached an asymptote
based on the sampling effort. A one-way analysis of
variance (ANOVA), followed by Tukeys multiple
comparison test, was performed to compare vertebrate
species richness, the number of generalist and spe-
cialist species between the two deforestation patterns
and the control areas. Non-metric multidimensional
scaling (NMDS) ordinations were performed based on
the Jaccard similarity matrix of vertebrate-species
occupancy of all landscape units to verify the similar-
ity in the overall vertebrate community composition,
and the generalist and specialist communities for the
studied landscapes. To test the significance of any
difference in the community composition between
landscapes, we conducted an analysis of similarity
(ANOSIM) with 10,000 permutations. SIMPER anal-
ysis was used to identify which species contributed
most to the observed community differences in the
study landscapes. For the ANOSIM and SIMPER
analyses we used the software PRIMER version 5.2.1.
To detect potential spatial autocorrelation, we
computed a Mantel test based on 5,000 permutations
using the straight-line distances among the 21 land-
scapes (measured from the central point of the
landscape unit) and a Jaccard dissimilarity matrix.
There was a significant spatial autocorrelation
between the community composition of vertebrates
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across all units (Mantel test, r = 0.18, p \ 0.05),
suggesting that closer landscapes had more similar
vertebrate communities. To take into consideration
this spatial autocorrelation we used the geographic
coordinates of each studied landscape in the multiple
regression analysis (see below).
To assess the relationship between species richness
and landscape variables we performed multiple
regression models. Model fitting was done using
generalized linear models (GLM), with a Poisson
family error distribution (base package in R v.
2.1.0.1; R Development Core Team 2008). We
conducted an exploratory data analysis to select only
those explanatory variables with a relatively low
correlation (Pearsons r \ 0.70; Zuur et al. 2009;
Supplementary Table S2).
We built two null modelsone where the species
richness was constant, with no influence of the
predictor variables, and a geographic model (due to
the spatial autocorrelation indicated by the Mantel
test), where the geographic coordinates were analyzed
with the response variables. We used latitude and
longitude in the null models, to test if in isolation they
were strong predictors of species richness. We found
that the longitude coordinate was more significant
(Z value = -2.19; p \ 0.05) than the latitude
(Z value = 0.55, p = 0.58).
To test predictions from four main hypothesis used
to explain patterns of vertebrate species richness we
built 38 GLMs. The four main hypotheses whose
factors affect species richness were as follows: land-
scape variables (forest proportion and number of
fragments), the regional context (size of the largest
connected patch), temporal variables (isolation age and
deforestation age), and their interactions. We devel-
oped these models with and without the longitude
coordinates (Supplementary Table S3). The size of the
largest patch structurally connected with the fragments
inside our 4 9 4 km landscapes was log transformed.
We conducted a maximum likelihood model
selection procedure, considering the second-order
Akaikes information criterion, corrected for small
sample sizes (AICc) (Burnham and Anderson 2002).
With this approach, the lower the AICc, the better the
model fits the data. We also calculated the difference
between AICc for all the models and the lowest
observed AICc. According to Burnham and Anderson
(2002), models with DAICc \ 2 are equally plausible
to explain the observed pattern as the best model. We
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Landscape Ecol (2012) 27:799812
also calculated the Akaikes information criteria
weight (wAICc), which expresses the relative contri-
bution of the model to explain the observed pattern
(Burnham and Anderson 2002), and the evidence ratio
of each model and the relative importance of the
predictor variables. We used the concurrent model
approach, and only the results for the best equally
plausible models (DAICc \ 2) are shown (Table 3)
(Burnham and Anderson 2002).
Results
Structural pattern and disturbance
The fish-bone pattern was associated with a more
fragmented landscape when compared to the large-
property pattern. Similarly, fish-bone landscapes were
isolated for longer when compared with large-proper-
ties and control areas that still retain connected forest
habitat (Table 1). Fish-bone landscapes were also
characterized by high levels of logging, burning, and
hunting disturbances, whereas large properties pre-
sented moderate hunting and low logging and burning
disturbances. Control areas presented the lowest
disturbance levels among the three landscape patterns
(Table 1).
Species richness and community structure
Species accumulation curves reached an asymptote,
indicating that the number of interviews conducted in
each landscape unit was sufficient to estimate the
species richness (Fig. 2).
We found the greatest number of vertebrate species in
control areas, followed by the large-property pattern and
the fish-bone pattern (Table 1). A similar result was
found for the number of specialist species present in
these landscape units (Table 1). When comparing the
generalist species, differences were only found between
the fish-bone landscapes and the control areas (Table 1).
Of the seven fish-bone landscapes studied, four had a
mean isolation age of 12 years (range 1113 years;
Landscapes FB 14 in Fig. 1) and three (Landscapes FB
57 in Fig. 1) were still structurally connected with
fragments outside the 4 9 4 km landscapes. We found
more species in the three structurally connected fish-
bone landscapes (mean SD = 32.6 3.2, range =
2935, n = 3) compared with the isolated fish-bone
Landscape Ecol (2012) 27:799812 805

Table 1 Forest patch metrics, disturbance degree (0 = none, species, specialist species and generalist species obtained
1 = light, 2 = moderate, 3 = heavy and 4 = very heavy) and through interviews with local landowners for fish-bone pattern
number of medium-sized and large-bodied mammals and birds (FB), large-property pattern (LP) and control areas (CT)
(Mean SD) FB LP CT FB vs CT FB vs LP LP vs CT

Forest proportion (%) 24.2 8.1 26.8 9.7 99.6 0.3 *** NS ***
Number of fragments 86.0 12.8 43.3 13.13 1 0.0 *** *** ***
Regional largest connected 11,077 18353 2,52,200 246737 2,51,761 247243 * * NS
patch (ha)
Deforestation age (years) 17 6.4 18 9.0 0 0.0 *** NS ***
Isolation age (years) 6.8 6.5 0 0.0 0 0.0 ** ** NS
Hunting intensity 3.4 3 0.3 *** NS ***
Intensity of fire 2.3 1 0.3 * NS NS
Logging intensity 3.6 1.2 0 *** ** NS
Number of species 29 4.7 39 5.2 43 2.2 *** ** NS
Number of generalist species 24.1 2.7 27.1 3.2 29.8 1.7 ** NS NS
Number of specialist species 5.1 2.7 11.7 2.3 13.7 0.9 *** *** NS
NS not significant
Tukeys multiple comparison test * p \ 0.05, ** p \ 0.01, *** p \ 0.001,

landscapes (mean SD = 26.7 4.1, range = 2232,
n = 4), although this difference was not significant
(t test, p = 0.09).
NMDS ordinations supported the idea that the
compositions of large vertebrate communities from
control and large-property landscapes were more
similar to each other than to those from the fish-bone
pattern (Fig. 3). NMDS also showed that vertebrate
communities in all large-property landscapes were
similar. The same pattern occurred for control areas,
whereas communities within the fish-bone landscapes
were very heterogeneous when compared to each
other. This heterogeneity was particularly apparent
when we further subdivided fish-bone into structurally
isolated and connected landscapes.
The one-way ANOSIM confirmed differences
among the three studied landscapes for the overall
vertebrate community composition (R = 0.47; p =
0.0001), for generalists (R = 0.37; p = 0.0001), and
for specialists (R = 0.40; p = 0.0001). Pairwise com-
parisons between landscapes indicated that the com-
munity composition of fish-bone landscapes differed
significantly from control areas (R = 0.725; p =
0.0006) and large-properties (R = 0.741; p = 0.0006).
However, there was no significant difference between
vertebrate communities in the large-property and control
landscapes (R = 0.124; p = 0.09). The same result
was found for the generalist and specialist community
compositions (Supplementary Table S4).
SIMPER analysis (presenceabsence data) of the
overall vertebrate community composition confirmed
more similar communities among large-properties and
control landscapes (92.3%), while vertebrate commu-
nities of the fish-bone landscapes were less similar to
large-property and control landscapes (79.9 and 79.8%
respectively; Table 2). SIMPER analysis also showed
that the average similarity among all the fish-bone,
large-property and control landscapes was 83.1, 91.5,
and 94.6%, respectively.
Determinants of species richness and composition
Our information theoretic model selection analysis
showed that the number of fragments was the strongest
predictor affecting the persistence of all, generalist
and specialist species in the studied landscapes. There
was a clear negative linear relationship between the
number of fragments and the total and specialist
species richness, demonstrating that the number of
large vertebrate species in a landscape unit decreases
as the number of fragments increases. The models with
(i) the number of fragments and longitude, and (ii)
number of fragments and largest connected patch were
the best predictors of the total species richness

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Fig. 2 Number of species recorded in relation to the number of

interviews conducted in each deforestation pattern unit and
control area (FB fish-bone pattern; LP large-property pattern,
CT control area; the fish-bone landscapes 14 are isolated, and
the units 57 are still structurally connected with the surround-
ing forest)

(Table 3), with the number of fragments showing the

P
highest relative weight of evidence ( Wi = 0.76),
P
followed by longitude
P ( Wi = 0.52) and the largest
connected patch ( Wi = 0.44) (Table 4).
Three models predicted the occurrence of specialist
species, all of which included the number of frag-
ments, and this variable presented the highest relative
P
weight of evidence ( Wi = 0.95). The largest con-
nected patch was also present in all of the three Fig. 3 NMDS ordination based on a Jaccard similarity matrix
selected models and was the second most sup- analysis showing community responses of a mid to large bodied
P vertebrates, b generalist species and c specialist species to
ported variable ( Wi = 0.69). For this group of
P deforestation between the fish-bone pattern (FB), the large-
species,
P isolation age ( Wi = 0.34) and longitude property pattern (LP) and the control areas (CT). Stress values
( Wi = 0.39) were also selected in one of the three are 0.0064, 0.019 and 2.4 e-07, respectively. Co represents
concurrent models, but they had little support as the the three fish-bone landscapes that are still connected

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Table 2 SIMPER analysis

Landscapes DS (%) Species Contribution (%)
with the dissimilarity (DS)
observed between the LP vs CT 7.9 Dusky titi monkey (Callicebus moloch) 10.1
landscapes studied and the
species that most contribute Kinkajou (Potos flavus) 9.0
to these observed Giant armadillo (P. maximus) 9.0
differences Marbled wood-quail (Odontophorus gujanensis) 8.1
Marmoset (Mico argentata) 7.1
FB vs LP 21.2 Red brocked deer (M. americana) 6.0
Puma (Puma concolor) 6.0
Giant anteater (M. tridactyla) 5.9
Razor-billed curassow (M. tuberosa) 5.9
Giant otter (P. brasiliensis) 5.9
Grey deer (Mazama gouazoubira) 5.0
Jaguar (P. onca) 4.9
Dusky titi monkey (C. moloch) 4.5
White lipped peccary (T. pecari) 4.0
Dark-winged trumpeter (P. viridis) 4.0
Six banded armadillo (Euphractus sexcinctus) 4.0
FB vs CT 21.9 Jaguar (P. onca) 6.2
Red brocked deer (M. americana) 5.4
Puma (P. concolor) 5.4
Giant armadillo (P. maximus) 5.4
Giant anteater (M. tridactyla) 5.4
Razor-billed curassow (M. tuberosa) 5.4
Dark-winged trumpeter (P. viridis) 4.6
Grey deer (M. gouazoubira) 4.5
Crab eating raccoon (Procyon cancrivorus) 4.5
Giant otter (P. brasiliensis) 4.4
Kinkajou (P. flavus) 4.1
Marmoset (M. argentata) 4.0

estimate plus or minus the standard error overlaps zero
(Table 4).
Generalist species were predicted by seven concur-
rent models, and again the number of fragments
showed the highest relative weight of evidence
P
( Wi = 0.42). All other landscape variables had
little support (Table 4).
Discussion
The primary aim of this study was to test the
importance of landscape configuration for vertebrate
communities in landscapes with a low proportion of
remaining habitat (\30%). As previously observed by
Batistella et al. (2000) and Oliveira-Filho and Metzger
(2006) the fish-bone pattern comprised a more frag-
mented landscape. We also found that the fish-bone
pattern was associated with relatively high disturbance
levels and retained a lower number of vertebrate
species. The vertebrate community in fish-bone land-
scapes was dominated by generalist species, while the
large-property pattern retained a vertebrate commu-
nity more similar to the control areas, with the
presence of top predators and specialist species.
A key finding of our study is that the number of
fragments is the most important predictor of generalist
and specialist species richness, followed by the
regional context (size of the largest connected patch).
These results demonstrate that habitat configuration

123
808 Landscape Ecol (2012) 27:799812

Table 3 Selected models with DAICc \ 2 considered to explain the total richness, and the richness of specialist and generalist
species in two Amazonian deforestation patterns and control areas in Alta Floresta, MT, Brazil
Model Response variable Predictor variables AICc df DAICc Weight Evidence ratio

R21 Richness # fragments ? longitude 125 4 0.0 0.256 1

R8 Richness # fragments ? largest patch 127 4 2 0.009 2.7
RS8 Specialist richness # fragments ? largest patch 91.5 4 0.0 0.278 1
RS27 Specialist richness # fragments ? largest patch ? longitude 92.8 5 1.4 0.139 1.9
RS18 Specialist richness # fragments ? isolation age ? largest patch 93.2 5 1.7 0.118 2.3
RG21 Generalist richness # fragments ? longitude 107.4 4 0.0 0.136 1
RG7 Generalist richness Forest proportion ? largest patch 108 4 0.6 0.100 1.3
RG2 Generalist richness # fragments 108.8 3 1.4 0.068 1.9
RG20 Generalist richness Forest proportion ? longitude 109 4 1.5 0.063 2.1
RG10 Generalist richness Largest patch ? deforestation age 109.1 4 1.6 0.060 2.2
RG1 Generalist richness Forest proportion 109.1 3 1.7 0.058 2.3
RG12 Generalist richness Forest proportion ? isolation age 109.4 4 2 0.058 2.6

(fragmentation) and connectivity with adjacent frag-
ments are important for the maintenance of vertebrate
diversity in landscapes with a low (*25%) proportion
of suitable (i.e., forest) habitat. The studied landscapes
presented spatial autocorrelation, and as a conse-
quence longitude was also an important predictor of
species richness. A possible explanation for this
pattern is the presence of continuous forest areas in
the Northeast and Southwest regions of our study area,
reinforcing the importance of adjacent forest areas
(Fig. 1).
It is important to note that the proportion of forest
within a 4,000 m buffer around the edge of each
landscape unit was significantly and positively corre-
lated with the proportion of forest inside each
landscape (r = 0.73, p \ 0.01), and that the size of
the largest connected patch was only moderately
correlated with the proportion of forest in the
surrounding habitat (r = 0.42, p = 0.055). There-
fore, the effect of the surrounding region is not related
with the forest cover per se at a larger scale, but
should be more related to the degree of connectivity
of the fragments inside and outside of the study
region. The differences in species richness and
composition between isolated and connected fish-
bone landscapes also support the importance of
connectivity at this larger spatial scale. These results
confirm the importance of forest configuration both
inside and outside of our study landscapes (mainly
represented by fragmentation and connectivity,
respectively) for vertebrate species.
Our results suggest that the loss of species and the
strong changes in the composition of the large
vertebrate community provoked by the fish-bone
pattern resulted from the high levels of fragmentation,
isolation, and disturbance observed in these land-
scapes. Previous studies have shown that the frag-
mentation and isolation of suitable habitat leads to a
reduction in population size and increased risk of
species extinction (Saunders et al. 1991). We found
that the influence of fragmentation was most apparent
for specialist species. In comparison, effect sizes for
generalist species were typically small and variable,
which prevents us from being able to define a clear
pattern of what predicts their occurrence. Community
changes resulting from habitat fragmentation result in
fewer species and a different species composition
compared with the original, unfragmented landscape
(McAlpine et al. 2006; Ockinger et al. 2010). These
general patterns were also found in previous studies in
our study region, where small isolated patches retained
fewer species of mammals (Michalski and Peres
2007) and birds (Lees and Peres 2006), than larger
fragments.
The main changes in the community structure of
fish-bone landscapes, when compared to the large-
property and control areas, are primarily shaped by
deletions of forest specialist species (Lees and Peres
2006), such as jaguars (P. onca), red brocked deer (M.
americana), giant armadillo (Priodontes maximus),
dark-winged trumpeter (Psophia viridis) and giant
otter (Pteronura brasiliensis) (Table 2). Only the

123
Landscape Ecol (2012) 27:799812 809

-0.010 0.045
0.022 0.055
-0.099 0.170
Table 4 Model weight and parameter (slope) estimates from informationtheoretic analysis of the species richness (R), specialist species richness (RS) and generalist species
connected fish-bone landscapes were able to maintain

Wi Slope (SE)
some specialist species such as giant armadillo

Deforestation age
(P. maximus), giant anteater (Myrmecophaga tridac-
tyla), red brocked deer (M. americana) and razor-
billed curassow (Mitu tuberosa). Despite the number
of species found in the connected fish-bone land-

0.158
0.191
0.197
P scapes, we did not record any top predators (jaguar and
puma), which suggests that the landscape configura-
-0.057 0.116
-0.097 0.152
-0.053 0.124
tion formed by the fish-bone pattern may not be
Wi Slope (SE)

adequate to maintain these species.

Temporal variables were relatively weak predictors
Isolation age

of the composition of vertebrate communities. The

very recent timing of deforestation (mean = 19.14;
0.252
0.348
0.246

range = 925 years) may have influenced this result.

P

Usually, species with long generation times will show

a delayed response to habitat loss (Tilman et al. 1994).
0.070 0.123
0.009 0.018
0.169 0.241
Wi Slope (SE)

Such a delay in response could explain why we still

Forest proportion

found some specialist species in isolated fish-bone

landscapes that have a deforestation age of approxi-
mately 20 years (range 2123 years). For example the
0.168
0.023
0.336

spider monkey (Ateles sp.) has a long life span

P

(3040 years) (Nowak 1999), and is slow to reproduce

-0.188 0.204
-0.098 0.141
-0.113 0.177

(Milton 1981). These life-history characters mean that

long-lived primates, such as the spider monkey, can
Wi Slope (SE)

persist in some small fragments for extended periods

([40 years) before they become extinct (Melo et al.
2005). Therefore, it is possible that in our isolated fish-
Longitude

bone landscapes, the relaxation time (the time taken by

0.524
0.396
0.379

a disturbed system to reach equilibrium; Diamond

P

1972) since isolation was likely insufficient to extin-

0.182 0.242
0.289 0.232
0.120 0.198

guish several taxa. These temporal delays mean that

Wi Slope (SE)

future extinctions in the fish-bone landscapes look

The Wi (Akaike weight) for all models with a given variable

certain, which will further exacerbate differences

Largest patch

between the community compositions of these defor-

estation patterns.
0.446
0.692
0.360

One possible confounding factor that operates

P

synergistically with habitat fragmentation to drive

richness (RG) for all 21 landscapes studied

-0.531 0.289
-0.598 0.179
-0.223 0.290

changes in vertebrate communities is hunting pressure

Number of fragments
Wi Slope (SE)

(Peres 2001). Although the hunting intensity in our

two Amazonian deforestation patterns was similar, the
higher fragmentation and the large number of small
farms around fragments in the fish-bone pattern may
0.767
0.959
0.421

have also contributed to the decline of species, as

P

fragments are more accessible to hunters (Cullen et al.

2000; Peres 2001). Hunting can thus affect a greater
Model

range of species and in many cases accelerate the

2
3
7

negative effects of fragmentation by driving popula-

Groups

tions to local extinction before the faunal relaxation

RG
RS

process is completed and new equilibrium conditions

R

123
810
are reached (Peres 2001). Control areas had few
people living around the properties, and were also
located far from the city, with a small number of roads,
which contributed to the low levels of anthropogenic
disturbance in these areas.
Results from our information theoretic model
selection demonstrated that differences between land-
scape units were driven primarily by different forest
configurations within the study units and that hunting
pressure and or other disturbances (such as logging
activity) can intensify those differences. Our results
support the idea that not only is the loss of habitat
important, but also the configuration of the landscape
after fragmentation contributes to the local extinction
of species, especially the extinction of forest-specialist
species. Landscape configuration likely affects species
persistence (Flather and Sauer 1996), with increased
fragmentation and loss of connectivity leading to
communities dominated by generalist species
(Lindenmayer et al. 2000; Laurance et al. 2002; Lees
and Peres 2006; McAlpine et al. 2006; Urquiza-Haas
et al. 2009). Such changes in the vertebrate assem-
blage can potentially have broader effects on the forest
ecosystem such as changes in predation, herbivory and
seed dispersal (Laurance et al. 2005).
Over time, fragmented communities will become
increasingly dominated by matrix-tolerant generalists,
disturbance-adapted opportunists, and species with
small area requirements (Laurance et al. 2002; Norris
et al. 2008), like the ones found in isolated fish-bone
landscapes. Fragmentation and the time since isolation
probably work together to limit the number of species
and to provoke the extinction of specialist species in
fish-bone landscapes. Future local extinctions in the
fish-bone pattern appear to be certain, but the fact that
recently isolated fragments are already facing a
decline in species richness emphasizes how fast this
pattern of deforestation affects the structure of the
large vertebrate community. The principal advantage
of the large-property pattern is that large forest
fragments are preserved, which favors specialist
species with larger area requirements.
Conservation implications
Combating deforestation in Brazil is a priority
for government action and international assistance
(Fearnside 2005) and new conservation strategies
123
Landscape Ecol (2012) 27:799812
must be implemented or the Amazon will be reduced
to islands of forest surrounded by pastures and other
agricultural areas (Fearnside 2001; Metzger 2001).
Conservation actions should occur inside private
lands. Planners must also consider the structural
differences among these typical Amazonian defores-
tation patterns while new colonization frontiers are
still being planned (Metzger 2001).
The greater number of specialist species we found
in the connected fish-bone landscapes and the results
of our regression models shows that the negative
impacts of this deforestation pattern can be at least
partially ameliorated by the retention of connections to
suitable (i.e., large) habitat areas (Metzger 2001;
Oliveira-Filho and Metzger 2006). If deforestation
could be spatially planned, maintaining forest rem-
nants in more aggregated blocks, with high levels of
connectivity, then fish-bone patterns could create
elongated areas of forest that would effectively cross
almost the entire landscape (Metzger 2001). Such
planning would contribute to a more sustainable
integration of biodiversity conservation within the
socioeconomic context.
Despite the existence of legislation that requires that
80% of the forest area must remain preserved in private
properties, in our study region many forest areas were
entirely cleared (before and after the legislation was
established) contributing to the isolation of the remain-
ing fragments (Michalski et al. 2010), especially in the
fish-bone landscapes. For these areas, programs of
reforestation (including the establishment of connec-
tions with large forest blocks) could, in the long term,
reduce the negative effects of anthropogenic change to
the landscape configuration. If legislation requiring the
retention of 80% forest cover were respected, inde-
pendent of the deforestation pattern, large forest
fragments and core areas would be maintained, with
high connectivity (Metzger 2001), which would allow
for the conservation of all forest species.
Acknowledgments This research was funded by the Wildlife
Conservation Society, Food and Health Foundation, Cleveland
Metroparks Zoo and The Rufford Small Grants Foundation. PP
was funded by the Brazilian Ministry of Education (CAPES)
Master studentship. FM was funded by a Fundacao de Amparo a
Pesquisa do Estado de Sao Paulo (FAPESP: 2007/01252-2)
post-doctoral studentship. We would like to thank all
landowners in Alta Floresta and particularly Geraldo and Alex
Araujo for invaluable field assistance. Darren Norris provided
insights that greatly improved previous versions and also helped
during fieldwork.
Landscape Ecol (2012) 27:799812
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