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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 among the fish-bone, large-property, and control areas
species persistence are predicted to be most apparent (mean = 29.3, 38.8 and 43.5 respectively). Control areas
when remaining habitat cover is below 30%. We tested and large-properties tended to have a higher number of
this prediction by comparing vertebrate communities in specialist species (mean = 13.7, and 11.7, respectively),
21 landscapes located in the southern Amazonia, includ- when compared with the fish-bone pattern (5.1). Verte-
ing 7 control landscapes (*100% of forest cover) and 14 brate community composition in the control and large-
fragmented landscapes (4 9 4 km). The fragmented properties was more similar to one another than to those
landscapes retained similar proportions of forest of the fish-bone landscapes. The number of fragments
(*25%), but had contrasting configurations, resulting was the main factor affecting the persistence of species,
from two different deforestation patterns: the fish-bone being negatively associated with specialist species rich-
pattern common in small properties, and the large- ness. Species richness was also positively related with the
property pattern generally used by large ranchers. size of the largest fragment structurally connected to the
Vertebrates were surveyed in all landscapes in Febru- studied landscapes (i.e., a regional scale effect). Our
aryJuly 2009 with interviews (n = 150). We found a results demonstrated that the large-property pattern,
significant difference in reported species richness which results in less fragmented landscapes, can maintain
a more diverse community of large vertebrates, including
top predators, which are considered fundamental for
Electronic supplementary material The online version of
this article (doi:10.1007/s10980-012-9729-0) contains maintaining ecosystem integrity. These results support
supplementary material, which is available to authorized users. the hypothesis that landscape configuration contributes to
the persistence and/or extirpation of species.
P. R. Prist (&)  J. P. Metzger
Department of Ecology, Bioscience Institute, University
of Sao Paulo, Rua do Matao, 321, Travessa 14, Sao Paulo, Keywords Large vertebrates  Deforestation
SP 05508-900, Brazil patterns  Landscape ecology  Landscape
e-mail: pprist@hotmail.com configuration  Species persistence  Brazilian Amazon
F. Michalski
Postgraduate Programme in Tropical Biodiversity, Federal
University of Amapa, Rod. Juscelino Kubitschek, km 02, Introduction
Macapa, AP 68902-280, Brazil
Habitat loss and fragmentation have been the two main
F. Michalski
Pro-Carnvoros Institute, Av. Horacio Neto, 1030, consequences of the intense human pressure experi-
Atibaia, SP 12945-010, Brazil enced in the tropics in recent decades (Bernard and

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Fenton 2007). They both cause isolation of remnant ca. 23 ha per year (Fujisaka et al. 1996). In contrast,
forest patches, thereby increasing risks of extinction the large-property pattern is characterized by rapid
(Bodmer et al. 1997; Laurance et al. 2011) and deforestation over large areas ([1,000 ha), and is
reducing native species richness (Stratford and Stouf- primarily caused by livestock farmers (Ferraz et al.
fer 1999; Cullen et al. 2000; Ferraz et al. 2007). 2005; Michalski et al. 2008). Both patterns cause
Fragmentation can be understood as a modification in fragmentation and habitat loss, but the remaining
the spatial arrangement of habitat patches, where a habitat patches have different configurations and
large expanse of habitat is transformed into smaller temporal dynamics. The fish-bone pattern usually
patches, resulting in many different spatial patterns results in forest remnants that are smaller, more
(Fahrig 2003). Habitat fragmentation reflects one irregular and less connected when compared to the
aspect of habitat configuration, and fragmentation large-property pattern (Oliveira-Filho and Metzger
effects are distinct from habitat loss (Swift and 2006).
Hannon 2010). The Amazon forest is one of the most extensive
Despite an extensive literature showing the impor- tropical forests of the world (Ferraz et al. 2005), and
tance of patch area and habitat loss to predict the deforestation, fragmentation and degradation of hab-
persistence of species, there are few studies discussing itat pose major threats to Amazon biodiversity (Lau-
the consequences of habitat configuration for main- rance et al. 2002; Peres et al. 2010). Mammals are
taining biodiversity in fragmented landscapes. Accord- among the most threatened species, being particularly
ing to the literature and previous empirical studies, it is sensitive to habitat loss and fragmentation (Linden-
expected that population size should be related to mayer et al. 2000). Birds are another vertebrate group
habitat loss in landscapes with a high proportion that are good indicators of disturbance in tropical
([30%) of habitat, while in landscapes below this forests, responding to changes in local vegetation
threshold, the configuration of habitat patches should structure and landscape scale processes, as well as
more intensively influence species richness and/or having an important role in forest regeneration (Bar-
population size (Andren 1994; Fahrig 1998). As a low and Peres 2006).
consequence, habitat configuration is expected to be Previous studies revealed negative effects of loss
more important for population persistence in land- and/or isolation of Amazonian forest remnants on the
scapes in which small amounts of the original habitat species richness of medium-sized and large-bodied
remain (Fahrig 1998). In this situation one should ask vertebrates (Stratford and Stouffer 1999; Laurance
the following question: which habitat configuration is et al. 2002; Lees and Peres 2006; Michalski and Peres
more suitable to maintain biodiversity? 2007). However, while some species for example
Studies of landscapes resulting from different larger bodied carnivores and primates (Michalski and
deforestation patterns are necessary to understand Peres 2005; Michalski et al. 2006), are lost from small
the influences of habitat configuration on patterns of and isolated habitat patches due to low densities, large
species persistence and community dynamics. Defor- spatial requirements, and conflicts with humans, other
estation patterns can be defined according to the size species may persist in relatively small forest patches
and spatial distribution of deforested areas (Oliveira- (Lees and Peres 2006; Michalski and Peres 2007). The
Filho and Metzger 2006). In the Brazilian Amazon, responses of medium-sized and large-bodied verte-
two different patterns can be easily identified, the brates to habitat disturbance and deforestation are thus
fish-bone pattern and the large-property pattern not completely understood.
(Oliveira-Filho and Metzger 2006). The fish-bone In this study we examined how the structural
pattern is common to small properties (usually 50 ha differences between two contrasting deforestation
in the Alta Floresta regionOliveira-Filho and Metz- patterns (fish-bone and large-property) in the Brazilian
ger 2006), which have been regularly distributed along Amazon affected the community composition and
roads. Such small properties were donated to small richness of medium-sized and large-bodied verte-
farmers (Ferraz et al. 2005) by the Brazilian Govern- brates. The studied landscapes had proportions of
ment colonization program in the 1970s (Metzger remaining forest habitat (ca. 25%) just below the
2001). These small family farmers gradually erode threshold where configuration effects should be more
the remaining forest on their properties, deforesting apparent. We used multi-model inference to identify

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relationships between the landscape structure and (continuous forest with [1,600 ha). Fish-bone and
vertebrate species richness to understand the relative large-property landscapes were selected based on a
importance of landscape components for maintaining visual inspection of the Landsat image (identified by
vertebrate diversity. Specifically, we linked interview their characteristic deforestation patterns, Oliveira-
data with forest patch metrics to test the hypotheses Filho and Metzger 2006) with approximately 25% of
that (1) the fish-bone pattern retains a smaller number forest cover (calculated from the classified image in
of total and specialist species and (2) the fish-bone ArcGIS version 9.2; ESRI 19992006). All grids were
pattern has a more negative effect on the community positioned within a regional context of similar forest
composition of large vertebrate community. cover patterns such that we avoided possible con-
founding effects of differences in bordering habitat
configurations. Access by paved and unpaved roads,
Materials and methods and permission provided by landowners (all land-
scapes were formed by private properties) were the
Study area and sampling design final criteria for the selection of the landscapes.
All the landscapes selected were composed of
This study was conducted in the region of Alta private properties that varied in size, but experienced
Floresta (09530 S, 56280 W), in the southern Brazil- the same type of land use: cattle ranching. Brazilian
ian Amazon (Fig. 1). The region is located in the law (the Brazilian Forest Act) requires that all private
center of the Arc of Deforestation, the contempo- properties in Brazilian Amazonia (independent of
rary epicenter of Amazon deforestation (Costa and size) should maintain 80% of the native vegetation of
Pires 2010). Alta Floresta has been subjected to high the property as legal reserve (Codigo Florestal 2001).
deforestation rates since the early 1980s (Michalski However, there is no concern about connectivity and
et al. 2008), resulting in a fragmented landscape these legal reserves do not follow any pre-deter-
containing forest patches of varying size, shape, and mined spatial plan. Despite this legal requirement,
degree of connectivity surrounded by a matrix of only a minority of private properties respects this law.
managed cattle pasture (Oliveira-Filho and Metzger Michalski et al. (2010) showed that from 300
2006), which is the dominant historic and present day landholdings surveyed in the Alta Floresta region,
land-use in Alta Floresta (Michalski et al. 2008, 2010). only 20.3% still retained 80% or more of the property
The annual average precipitation and temperature is area as native forest cover.
2,350 mm and 24.5C, respectively, with high relative
humidity (8085%; RADAM BRASIL 1983). Alti- Vertebrate surveys
tudes vary between 200 and 300 m. There is no
evidence to suggest that differences in forest cover Obtaining species occurrence data through local
between landscapes are due to abiotic conditions and interviews is an effective approach that has been
as recently as 1976, the Alta Floresta region was successfully tested with medium-sized and large-
entirely covered by undisturbed Amazonian forest of bodied vertebrates (Lawes et al. 2000; Michalski and
similar physiognomy (Oliveira-Filho and Metzger Peres 2005; Urquiza-Haas et al. 2009; Sampaio et al.
2006; Michalski et al. 2007). Therefore, we assume 2010). To estimate vertebrate species richness in the
that there is no variation in forest type and composition 21 landscapes we conducted 150 interviews with local
across the landscapes. This assumption is supported by landowners between February and July 2009 (fish-
the fact that present day forest cover comprises bone: mean SD = 8 3, range = 515; large-
primarily mature forests, as in this region there is property: 7 3, range = 512; control landscapes:
little secondary forest regeneration due to intensive 5 1, range = 58, interviews). Focal species were
cattle grazing (Michalski et al. 2008). restricted to medium-sized and large-bodied mammals
Twenty-one 4 9 4 km (1,600 ha) landscapes ([400 g) and birds ([200 g) that could be easily
were selected through the analysis of a georeferenced identified by landowners. In our study area, each
2008 Landsat TM image (scene 227/67) (Fig. 1). The of the fish-bone landscapes (4 9 4 km) encompassed
study landscapes comprised seven fish-bone pattern, approximately 40 properties, while the large-property
seven large-property pattern and seven control areas landscapes and control areas usually included less

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Fig. 1 The region of Alta Floresta with the 21 landscapes 2009 Landsat TM image. The fish-bone landscapes 14 are
sampled in this study. The dark grey, light grey and black areas isolated, whereas units 57 are still structurally connected with
represent forest, non-forest, and open water, respectively in a the surrounding forest

than 10 properties. Therefore, we interviewed a only two (1.33%) interviews (which we retained in our
random sample of landowners in the fish-bone land- analysis) suggesting a high level of reliability in our
scapes, while (almost) all landowners or land-manag- results. All species were reported only if they were
ers (when landowners did not live in the region) were present in the landscapes during the 5 years preceding
interviewed in the other landscape types. interviews, and a species was considered present only
To ensure that we obtained reliable answers all when 50% or more of the interviews reported it as
interviews were conducted with the assistance of a present in the same landscape unit. This method does
local resident, known in the community. As a not enable us to distinguish between resident or
prerequisite, interviewees were interviewed only if: transient species, thus we considered both as present in
(1) they were willing to be interviewed, (2) had the studied landscapes.
knowledge of the fauna of the region, and (3) had lived
in or near the property for at least 2 years. In all cases Within-patch disturbance and forest-patch metrics
the interviews were accompanied by color plates with
images (photos and drawings) of all species known to Fragmentation and deforestation are commonly asso-
exist in the region (Michalski and Peres 2005, 2007; ciated with many synergistic disturbances that can
Peres and Michalski 2006). To assess the frequency of transform fragments into entirely new ecosystems
type II errors, we included seven species known to be (Laurance et al. 2002, 2011; Peres and Michalski
entirely absent from the study region. From the total of 2006; Peres et al. 2010). To characterize the intensity
150 interviews, we detected false-positive records in and extent of disturbance within each landscape unit

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we used information obtained from the local land- to the fragments inside the 4 9 4 km studied land-
owner interviews. Logging intensity and burn severity scapes (hereafter referred to as largest connected
were classified using a five-point scale: (0) none, (1) patch).
light, (2) moderate, (3) heavy, and (4) very heavy. Our
measure of logging intensity took into account the Data analysis
method of timber extraction, selection of tree species,
the relative amount of harvested timber, and the Total species richness and the richness of generalist
number of years since the extraction stopped. Burn and specialist species were considered as response
severity (using the same five-point scale as above) variables and modeled separately in all further anal-
considered the proportion of forest that was burned yses. The classification of vertebrates into generalist
(edge or interior), and the number of fire occurrences (including: howler monkey, Alouatta seniculus; tayra,
(Michalski and Peres 2005). We also derived a Eira barbara; paca, Cuniculus paca) and specialist
qualitative hunting intensity index that included species (including: red brocked deer, Mazama amer-
information about the hunting history (frequency and icana; white-lipped peccary, Tayassu pecari; jaguar,
time since the last hunting event was recorded), the Panthera onca) was based on forest dependence and
hunting pressure (none, light, heavy), and if hunting characteristics such as hunter preferences that were
activities still took place when we conducted inter- obtained from an extensive literature review (see the
views (see supplementary online material for more complete species classification list in Supplementary
details). Table S1).
Landscape variables were extracted from a Landsat We constructed curves of mean species richness
image (July 28th, 2009) using Fragstats (version 3.3; incremented by the interview sampling effort, with the
McGarigal and Marks 1995) and ArcGIS (version 9.2; software EstimateS (Colwell 2005; version 7.5), to test
ESRI 19992006). We applied an unsupervised clas- whether species richness had reached an asymptote
sification to derive three land cover classes (forest, based on the sampling effort. A one-way analysis of
non-forest and water), and assessed the accuracy of the variance (ANOVA), followed by Tukeys multiple
classified land cover map by comparing the 2009 comparison test, was performed to compare vertebrate
classified image with 234 reference points obtained in species richness, the number of generalist and spe-
the field from February to July of 2009. This resulted cialist species between the two deforestation patterns
in 100% matching. and the control areas. Non-metric multidimensional
For each studied landscape we measured forest scaling (NMDS) ordinations were performed based on
proportion, number of fragments, and two temporal the Jaccard similarity matrix of vertebrate-species
variables: isolation age and deforestation age. These occupancy of all landscape units to verify the similar-
temporal variables were measured from 14 biannual ity in the overall vertebrate community composition,
Landsat-5 TM images (scene 227/67) dated from 1984 and the generalist and specialist communities for the
to 2009. The isolation age was defined as the number studied landscapes. To test the significance of any
of years since the studied landscape lost its structural difference in the community composition between
connectivity, i.e., when a forest patch does not span (or landscapes, we conducted an analysis of similarity
percolate) the entire extent of the landscape (Stauffer (ANOSIM) with 10,000 permutations. SIMPER anal-
1985). Deforestation age was defined as the number of ysis was used to identify which species contributed
years since the first event of deforestation could be most to the observed community differences in the
detected in the landscape unit from the Landsat scene. study landscapes. For the ANOSIM and SIMPER
All images used to derive these temporal variables analyses we used the software PRIMER version 5.2.1.
were aligned and georeferenced using the 2008 To detect potential spatial autocorrelation, we
Landsat image as a base. We used at least 19 points computed a Mantel test based on 5,000 permutations
to align the images, resulting in a positional error of using the straight-line distances among the 21 land-
less than one pixel (mean SD = 25.40 2.64 m). scapes (measured from the central point of the
To consider the landscape context at a broader landscape unit) and a Jaccard dissimilarity matrix.
(regional) spatial scale, we also measured the size of There was a significant spatial autocorrelation
the largest forest area that was structurally connected between the community composition of vertebrates

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across all units (Mantel test, r = 0.18, p \ 0.05), also calculated the Akaikes information criteria
suggesting that closer landscapes had more similar weight (wAICc), which expresses the relative contri-
vertebrate communities. To take into consideration bution of the model to explain the observed pattern
this spatial autocorrelation we used the geographic (Burnham and Anderson 2002), and the evidence ratio
coordinates of each studied landscape in the multiple of each model and the relative importance of the
regression analysis (see below). predictor variables. We used the concurrent model
To assess the relationship between species richness approach, and only the results for the best equally
and landscape variables we performed multiple plausible models (DAICc \ 2) are shown (Table 3)
regression models. Model fitting was done using (Burnham and Anderson 2002).
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 Results
conducted an exploratory data analysis to select only
those explanatory variables with a relatively low Structural pattern and disturbance
correlation (Pearsons r \ 0.70; Zuur et al. 2009;
Supplementary Table S2). The fish-bone pattern was associated with a more
We built two null modelsone where the species fragmented landscape when compared to the large-
richness was constant, with no influence of the property pattern. Similarly, fish-bone landscapes were
predictor variables, and a geographic model (due to isolated for longer when compared with large-proper-
the spatial autocorrelation indicated by the Mantel ties and control areas that still retain connected forest
test), where the geographic coordinates were analyzed habitat (Table 1). Fish-bone landscapes were also
with the response variables. We used latitude and characterized by high levels of logging, burning, and
longitude in the null models, to test if in isolation they hunting disturbances, whereas large properties pre-
were strong predictors of species richness. We found sented moderate hunting and low logging and burning
that the longitude coordinate was more significant disturbances. Control areas presented the lowest
(Z value = -2.19; p \ 0.05) than the latitude disturbance levels among the three landscape patterns
(Z value = 0.55, p = 0.58). (Table 1).
To test predictions from four main hypothesis used
to explain patterns of vertebrate species richness we Species richness and community structure
built 38 GLMs. The four main hypotheses whose
factors affect species richness were as follows: land- Species accumulation curves reached an asymptote,
scape variables (forest proportion and number of indicating that the number of interviews conducted in
fragments), the regional context (size of the largest each landscape unit was sufficient to estimate the
connected patch), temporal variables (isolation age and species richness (Fig. 2).
deforestation age), and their interactions. We devel- We found the greatest number of vertebrate species in
oped these models with and without the longitude control areas, followed by the large-property pattern and
coordinates (Supplementary Table S3). The size of the the fish-bone pattern (Table 1). A similar result was
largest patch structurally connected with the fragments found for the number of specialist species present in
inside our 4 9 4 km landscapes was log transformed. these landscape units (Table 1). When comparing the
We conducted a maximum likelihood model generalist species, differences were only found between
selection procedure, considering the second-order the fish-bone landscapes and the control areas (Table 1).
Akaikes information criterion, corrected for small Of the seven fish-bone landscapes studied, four had a
sample sizes (AICc) (Burnham and Anderson 2002). mean isolation age of 12 years (range 1113 years;
With this approach, the lower the AICc, the better the Landscapes FB 14 in Fig. 1) and three (Landscapes FB
model fits the data. We also calculated the difference 57 in Fig. 1) were still structurally connected with
between AICc for all the models and the lowest fragments outside the 4 9 4 km landscapes. We found
observed AICc. According to Burnham and Anderson more species in the three structurally connected fish-
(2002), models with DAICc \ 2 are equally plausible bone landscapes (mean SD = 32.6 3.2, range =
to explain the observed pattern as the best model. We 2935, n = 3) compared with the isolated fish-bone

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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, was found for the generalist and specialist community
n = 4), although this difference was not significant compositions (Supplementary Table S4).
(t test, p = 0.09). SIMPER analysis (presenceabsence data) of the
NMDS ordinations supported the idea that the overall vertebrate community composition confirmed
compositions of large vertebrate communities from more similar communities among large-properties and
control and large-property landscapes were more control landscapes (92.3%), while vertebrate commu-
similar to each other than to those from the fish-bone nities of the fish-bone landscapes were less similar to
pattern (Fig. 3). NMDS also showed that vertebrate large-property and control landscapes (79.9 and 79.8%
communities in all large-property landscapes were respectively; Table 2). SIMPER analysis also showed
similar. The same pattern occurred for control areas, that the average similarity among all the fish-bone,
whereas communities within the fish-bone landscapes large-property and control landscapes was 83.1, 91.5,
were very heterogeneous when compared to each and 94.6%, respectively.
other. This heterogeneity was particularly apparent
when we further subdivided fish-bone into structurally Determinants of species richness and composition
isolated and connected landscapes.
The one-way ANOSIM confirmed differences Our information theoretic model selection analysis
among the three studied landscapes for the overall showed that the number of fragments was the strongest
vertebrate community composition (R = 0.47; p = predictor affecting the persistence of all, generalist
0.0001), for generalists (R = 0.37; p = 0.0001), and and specialist species in the studied landscapes. There
for specialists (R = 0.40; p = 0.0001). Pairwise com- was a clear negative linear relationship between the
parisons between landscapes indicated that the com- number of fragments and the total and specialist
munity composition of fish-bone landscapes differed species richness, demonstrating that the number of
significantly from control areas (R = 0.725; p = large vertebrate species in a landscape unit decreases
0.0006) and large-properties (R = 0.741; p = 0.0006). as the number of fragments increases. The models with
However, there was no significant difference between (i) the number of fragments and longitude, and (ii)
vertebrate communities in the large-property and control number of fragments and largest connected patch were
landscapes (R = 0.124; p = 0.09). The same result 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 Batistella et al. (2000) and Oliveira-Filho and Metzger
(Table 4). (2006) the fish-bone pattern comprised a more frag-
Generalist species were predicted by seven concur- mented landscape. We also found that the fish-bone
rent models, and again the number of fragments pattern was associated with relatively high disturbance
showed the highest relative weight of evidence levels and retained a lower number of vertebrate
P
( Wi = 0.42). All other landscape variables had species. The vertebrate community in fish-bone land-
little support (Table 4). scapes was dominated by generalist species, while the
large-property pattern retained a vertebrate commu-
nity more similar to the control areas, with the
Discussion presence of top predators and specialist species.
A key finding of our study is that the number of
The primary aim of this study was to test the fragments is the most important predictor of generalist
importance of landscape configuration for vertebrate and specialist species richness, followed by the
communities in landscapes with a low proportion of regional context (size of the largest connected patch).
remaining habitat (\30%). As previously observed by These results demonstrate that habitat configuration

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

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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 Landscape Ecol (2012) 27:799812

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

123
Landscape Ecol (2012) 27:799812 811

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