The Cerrado into-pieces: Habitat fragmentation as a function of landscape

use in the savannas of central Brazil

Fbio M.V. Carvalho
a
, Paulo De Marco Jnior
a,
*
, Laerte G. Ferreira
b
a
Laboratrio de Ecologia Terica e Sntese, Departamento de Biologia Geral, Instituto de Cincias Biolgicas, Universidade Federal de Gois, Brazil
b
Laboratrio de Processamento de Imagens e Geoprocessamento, Instituto de Estudos Scio-Ambientais, Universidade Federal de Gois, Brazil
a r t i c l e i n f o
Article history:
Received 2 July 2008
Received in revised form 23 January 2009
Accepted 29 January 2009
Available online 6 March 2009
Keywords:
Biodiversity conservation
Landscape structure
Fragmentation indices
Land-use patterns
a b s t r a c t
Habitat fragmentation and land conversion by humans for agricultural purposes are constant threats to
conservation of biodiversity in the Cerrado biome. These landscapes dominated by agricultural activities
became dynamic mosaics, which are formed by different land uses. Thus, understanding how the prop-
erties of these mosaics affect species persistence is one urgent necessity. In this study, the landscape
structure of the Cerrado in Gois State, Central Brazil, was quantied by the use of fragmentation indices,
analysed at the class level. The objective of this study was to assess if land use for crop production or for
pasture produces different fragmentation patterns, which can result in different pressures for the Cerrado
biodiversity. The study showed that landscapes dominated by crops are more fragmented than land-
scapes dominated by pastures. These crop-dominated landscapes also presented a smaller number of
fragments that could maintain populations of threatened mammal species in Cerrado. Regions with more
preserved natural areas are in the northeast of Gois, where there are rough relief and soil unsuitable for
agriculture. Our results indicate that croplands generate a landscape structure more damaging for the
conservation of biodiversity in the Cerrado biome. Otherwise, they support the importance to preserve
natural remnants, even in areas occupied by agriculture, mainly due to its potential to maintain ecosys-
tem services, and suggest that landscapes dominated by pastures should have more current value for
conservation, since they showed larger fragments.
2009 Elsevier Ltd. All rights reserved.
1. Introduction
Landscapes dominated by agriculture and pastures usually are
mosaics that include other land uses, such as urban areas, roads,
water courses and patches of natural vegetation (Bennett et al.,
2006). These mosaics offer a variety of habitat types for animal
and plant species, that can be restricted to the natural elements
of the landscape or be capable to use the human-altered areas.
These landscapes are dynamic units that change their structure
continuously, suffering habitat loss and fragmentation, but also
recovering marginal areas. The effects of these changes on natural
communities seem predictable, since we have information about
the life history and dispersal capability of the organisms under
consideration, as well as on the spatial structure parameters re-
lated to the modications occurring in the landscape (Burel et al.,
2004).
Habitat fragmentation is often dened as a process in which an
extension of the habitat is transformed into a number of small
patches, with smaller total area, and isolated from each other by
a matrix different from the original habitat. The above denition
obviously merge the effects of habitat loss (amount of area remain-
ing) and habitat fragmentation per se (amount of habitat sub-divi-
sion and isolation), which may hind the interpretation of its effects
on natural communities (Fahrig, 2003). Some studies suggest that
habitat loss has stronger negative effects on biodiversity, compar-
atively to isolation, whose effects, besides weaker, can be either
negative or positive (Fahrig, 2003).
This denition implies in four effects regarding habitat patterns,
which form the basis of most of the quantitative fragmentation
measures: (a) reduction in habitat amount; (b) increase in number
of patches; (c) reduction in patch size; and (d) increase of isolation
between patches (Fahrig, 2003). The fragmentation, however, is
not a random process, and it occurs preferably in areas where agri-
culture activities become more protable (Baldi et al., 2006). It is
expected that each economic activity that competes with native
vegetation for space (including different agriculture commodities,
cattle raising, mining and urban settlements) is subject to optimal
topographic and landscape characteristics to its development
(Gautam et al., 2003; Grau et al., 2005; Baldi et al., 2006). Likewise,
such human activities also demand different modications in the
landscape (e.g. different needs for roads, different forms of spatial
structure of habitat remnants), which may be associated to differ-
ent fragmentation patterns (Torbick et al., 2006).
0006-3207/$ - see front matter 2009 Elsevier Ltd. All rights reserved.
doi:10.1016/j.biocon.2009.01.031
* Corresponding author. Tel.: +55 62 35211480.
E-mail address: pdemarco@icb.ufg.br (P. De Marco).
Biological Conservation 142 (2009) 13921403
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At present, there is a growing amount of evidence that supports
the importance of agriculture-dominated landscapes for conserva-
tion of a set of biodiversity elements (Potts et al., 2006; Vander-
meer and Perfecto, 2007). These areas can maintain a vegetation
structure with more permeability in the matrix among fragments;
thus, the individuals can move more easily, what contributes for
the processes of recolonisation and maintenance of genetic diver-
sity. A landscape mosaic approach consider these landscapes as a
spatially complex and heterogeneous structure, formed by differ-
ent types of patches and where the matrix contains different types
of habitats, more or less favourable to the species of the natural
habitat considered (Metzger, 1999). Therefore, the matrix of these
areas should not be seen simply as a hostile environment, but as an
area that could be managed to contribute to the conservation of
biodiversity even in areas where most of the natural habitat has al-
ready been converted (Vandermeer and Perfecto, 2007).
We consider that habitat fragmentation, more specically area
and isolation, should be used as surrogates for the probability of
persistence of many threatened species. Many studies demon-
strated that population size is one of the most efcient predictors
of extinction risk (OGrady et al., 2004; Fagan and Holmes, 2006),
especially for large species (Cardillo et al., 2005). This suggests that
the area available for colonisation may be a good predictor for spe-
cies persistence, since large and connected areas will probably
maintain large populations. We assume that probability of persis-
tence is a function of the maximum attainable abundance in a frag-
ment and this vary among species due to their bionomic
characteristics, as habitat and diet specialization or body size (Da-
muth, 1981; Promislow and Harvey, 1990; Kelt and Van Vuren,
1999; Jetz et al., 2004; Fernandez and Vrba, 2005). In mammals,
especially those with territorial behaviour, a crude estimate for this
maximum abundance could be made using the mean home range
of individuals or groups (in social species) for a focal species and
this was used for many conservation purposes (Kirk and Bathe,
1994; MacDonald and Rushton, 2003; Jetz et al., 2004). Thus, the
distribution of fragment areas is expected to be a useful surrogate
for the probability of persistence in a given landscape. Considering
the lack of distributional information of many threatened species,
especially in tropical areas of the world (Nelson et al., 1990; Kuper
et al., 2006; Tobler et al., 2007), the fragmentation pattern is a cost-
effective surrogate for species persistence and may be useful to
evaluate the differences among land-use strategies in respect to
biodiversity conservation.
The Cerrado biome is located in central Brazil, and has an area
of about 2 million km
2
, which corresponds to approximately 25%
of the Brazilian territory (IBGE, 2004). The Cerrado is formed by
different vegetation physiognomies, from savanna-like formations
to forest forms, like gallery forests (Eiten, 1982; Redford and
Fonseca, 1986). The Cerrado biome presents a high species rich-
ness and high endemism of plants and vertebrates (Myers et al.,
2000; Colli et al., 2002; Klink and Machado, 2005) and is under
a rapid process of conversion to soya and maize plantation, exten-
sive cattle raising (Klink and Moreira, 2002; Klink and Machado,
2005), and an imminent expansion of sugar cane plantations. Cur-
rently, about of 39% of its total area is under non-Cerrado land
cover (Sano et al., 2008), although Machado et al. (2004) consider
a worst scenario with approximately 55% of Cerrado converted to
other land cover classes. This difference is probably related to
divergences in the identication of native pastures and natural
or altered areas. Moreover, only 2% of Cerrado area is inside pro-
tected areas (Klink and Machado, 2005). Due to its high ende-
mism and strong human pressure, the Cerrado is considered
one of the hotspots for the conservation of biodiversity in the
world (Myers et al., 2000).
In face of the rapid land use changes that resulted from agricul-
ture development and human population growth (Tilman et al.,
2001), it is urgent to understand how the properties of the land
use mosaics inuence the persistence of animal and plant popula-
tions and the maintenance of ecological processes. A recent analy-
sis of the Cerrado areas on Mato Grosso and Bahia in Brazil showed
that there is a relation between slope, land tenure and vegetation
dynamics with the fragmentation pattern (Brannstrom et al.,
2008), but the core area of Cerrado of Gois was not analysed. Thus,
it is fundamental to provide a predictive view of the relations be-
tween human activities and the parameters that describe habitat
fragmentation that are directly related to biodiversity conserva-
tion. In this study we analyse the landscape structure in Gois,
the only Brazilian state thoroughly within the Cerrado biome, test-
ing if landscapes dominated by pastures or by crops differ in their
fragmentation patterns, and how they could be predictable from
other environmental variables. Additionally, we highlight the con-
servation value of the Cerrado remnants evaluating the potential
occurrence of some threatened mammal species based on some
simple assumptions about their expected densities based on home
range estimates. Under this approach we compare the potential
occurrence of jaguar (Panthera onca), pampas cat (Leopardus colo-
colo), bush dog (Speothos venaticus), giant anteater (Myrmecophaga
tridactyla), giant armadillo (Priodontes maximus) and maned wolf
(Chrysocyon brachyurus) in relation to land use patterns, hoping
to determine how future economic pressures to convert the Cerra-
do could affect these species. All these species are considered
threatened based on IUCN criteria in the Brazilian Red List (IBAMA,
2003).
2. Materials and methods
2.1. Environmental information
Terrain slope data was obtained from Hydro-1 K digital eleva-
tion model (http://edc.usgs.gov/products/elevation/gtopo30/hy-
dro/index.html), processed at the resolution of 0.041 decimal
degrees. Land cover information, regarding the distribution of both
native and converted Cerrado classes, was based on interpretation
of 2001 and 2002 Landsat ETM+ satellite images (Sano et al., 2008)
interpreted through a semi-automated data analysis strategy; i.e.
each 1 1.5 subscene was segmented (divided into groups of
adjacent and spectrally uniform pixels). The polygons generated
were then converted into shapele format and visually interpreted
on the computer screen by overlaying them on the corresponding
RGB ETM+ colour composites of bands 3, 4, and 5. The following
land cover classes were considered in this study: natural vegeta-
tion grasslands, shrublands, forestlands, and secondary growths
(capoeira); anthropic classes croplands, pasturelands, reforesta-
tions, urban areas, and mining areas. The overall accuracy, ana-
lysed in terms of two classes natural vegetation versus non-
Cerrado land cover was about 90%.
It is important to emphasize that the images used for mapping
the land cover classes were selected based on their radiometric
quality and absence of cloud cover (less than 10%). Thus, most
images were from the dry season months of 2002 (Sano et al.,
2007, 2008). Due to partial cloud cover, some scenes needed to
be replaced by 2001 acquisitions. If this was the case, the over-
passes selected were also from the dry season months. Thus, the
conspicuous seasonality/phenology of the Cerrado biome did not
have a signicant impact on the discrimination of the land cover
classes.
The land cover mapping of the state of Gois (Fig. 1) was a major
effort (within the context of the project Identication of Priority
Areas for Biodiversity Conservation in Gois State), which con-
sisted in the interpretation of 23 Landsat scenes, extensive eld
work, and ancillary data (e.g. Radambrasil maps, agricultural cen-
sus data and terrain features). Certainly, this map will need to be
F.M.V. Carvalho et al. / Biological Conservation 142 (2009) 13921403 1393
updated soon, which has not been done yet. Nevertheless, the sys-
tematic deforestation assessments in the Cerrado region, based on
moderate resolution imagery, indicates that about 1105 km
2
of
new conversions took place in Gois from 2003 to 2007, less than
0.9% of the total remnant vegetation in the state; i.e. we can as-
sume that the major land cover spatial distribution patterns de-
tected from the 2002 Landsat imagery are still signicantly the
same.
2.2. Potential occurrence of threatened mammals
We assume that area is one of the most important factors deter-
mining the population size of mammals in the fragments. Habitat
quality may also be an important issue (Laidlaw, 2000), but we as-
sume that large areas present, in general, the most undisturbed
habitats at least due to lower edge effects (Dijak and Thompson,
2000; Parks et al., 2002; Pardini et al., 2005). Following this, we
consider that many fragments had an area that could not maintain
a minimum number of individuals, especially for large mammals
that require more area to maintain a territory. The lower area
threshold for occurrence is obviously different among species,
but it is expected to be at least well correlated to individual or
group (for social species) home range estimates.
We use the minimum area to maintain 10 non-overlapping
home ranges as a surrogate model for the potential occurrence of
selected mammal species in the fragments. This arbitrary number
was chosen only to exclude fragments that probably do not main-
tain persistent populations. We do not intent here to present pre-
cise viability estimates, but by using home range surrogates for
species presence, we devise a simple method to evaluate the con-
servation value of the fragments, even for species with poor life-
history information that preclude the use of more detailed viability
models.
We selected all the six terrestrial mammal species present in
Brazilian Red List (IBAMA, 2003) that occur in the Cerrado, exclud-
ing only the rodents for which there is limited information about
their home range. The home range estimates and their sources
for the species analysed are presented in Table 1. In all cases we
use the maximum home range estimate available from different
studies as a conservative procedure.
2.3. Data analysis
Our basic unit of analysis was a 0.5 latitude 0.5 longitude
cell in a grid that covers the entire Gois State. The more frequent
landscape units (pastures, croplands or cerrado) that represented
twice the proportion of the other units were considered dominant
in each cell. In cases where this criterion did not hold, the cell was
classied according to the prevalent landscape units as cerrado
pasture (cp), cerradocropland (ccr), croplandpasture (crp)
and cerradocroplandpasture (ccrp). For each cell, common
metrics of fragmentation structure (Gustafson, 1998; Metzger,
2003) were calculated using the software FRAGSTATS 3.3 (McGari-
gal and Marks, 1995). These metrics can be structural, when they
measure the spatial conguration of a landscape without an expli-
cit reference to some ecological process, or functional, when they
consider landscape patterns relevant to the functioning of a given
organism or process of interest. The metrics can be dened at three
levels of analysis: patch, class, and landscape (McGarigal and
Marks, 1995). In this study, we used only structural class metrics,
which are associated to all patches of a given type of habitat (class)
present in the landscape and measure the quantity and the spatial
conguration of each type of patch, providing a measure of
fragmentation.
Table 2 shows abbreviations of the metrics formulae used in
this study, while the indices are described in Table 3. The choice
of indices should consider that some of them can be highly corre-
lated (McGarigal and Marks, 1995; Hargis et al., 1998), so that their
use can yield redundant results. Therefore, the selection of a few
independent metrics may be more appropriate and sufcient to
identify landscape patterns (Riitters et al., 1995).
The relationship between landscape metrics and the dominant
land cover type in each landscape was performed by analysis of
variance (ANOVA), according to Zar (1999). In case of signicant
difference, it was used a Tukey a posteriori test, to determine which
comparison presents statistical difference. The statistical depen-
Fig. 1. Maps of Gois State, central Brazil: (a) land use and (b) slope (percent rise) and rivers. Percent rise of slope equals 100 when slope in degrees equals 45 and, as the slope
angle approaches 90, percent rise increases without limit. Higher values of percent rise indicate more sloping terrain.
1394 F.M.V. Carvalho et al. / Biological Conservation 142 (2009) 13921403
dence of fragmentation metrics at each land cover type to the pro-
portion of remnant habitat, under a habitat loss/habitat fragmenta-
tion framework (Andrn, 1994), was tested using linear regression
analysis according to Zar (1999).
3. Results
Landscapes dominated by natural vegetation are located mainly
in the Northeastern Gois in areas that present rougher and sloping
terrains. Landscapes dominated by crops occurred mainly in the
south and southwestern parts of the state (Fig. 2). Landscapes
dominated by pastures are spread across all of the central and wes-
tern areas of Gois, particularly in the Araguaia basin towards the
limits of the legal Amazon (Fig. 2).
Analysing the class level metrics, number of patches (NP) was
larger in landscapes dominated by crops than by pastures, and
these differences are not explained by chance (Fig. 3a). This index
was also larger in areas dominated by the mosaic croplandpasture
than in areas dominated by Cerrado. In relation to the percentage
of landscape index (PLAND), pasture areas showed larger values
than crop-dominated areas (Fig. 3b). As expected, Cerrado-domi-
nated landscapes showed larger values for PLAND (Fig. 3b) and
smaller values to edge density (ED). Signicant difference was ob-
served in ED values only between Cerrado and pasture (Fig. 3c).
There was no signicant difference for the patch area coefcient
of variation (AREA_CV) among any of the landscapes (Fig. 3d).
The shape indices, SHAPE_AM e SHAPE_SD, were signicantly lar-
ger in pasture areas than in cropland areas (Fig. 4a and b), indicat-
ing that fragments in pasture-dominated landscapes are more
irregular than fragments of the crop-dominated landscapes. The
shape index corrects the problem of dependence of patch area that
occurs in perimeter-area ratio, and so it is a simple measure and
one of the most used shape index. Radius of gyration area-
weighted mean (GYRATE_AM) was larger in landscapes dominated
by Cerrado, and also in areas of pasture, when compared to areas of
crops (Fig. 4c). The mean Euclidean nearest neighbour distance
Table 1
Home range sizes of selected threatened mammal species in Cerrado for occurrence modelling.
Species Maximum home range (ha) Source
Jaguar (Panthera onca) 110,100 Silveira (2004)
Pampas cat (Leopardus colocolo) 2770 Oliveira et al. (2008)
Bush dog (Speothos venaticus) 10,000 DeMatteo and Loiselle (2008)
Giant anteater (Myrmecophaga tridactyla) 4276 Miranda (2004)
Giant armadillo (Priodontes maximus) 1005 Silveira et al. (accepted for publication)
Maned wolf (Chrysocyon brachyurus) 11,500 Cheida et al. (2006)
Table 2
Variables and abbreviations used in the formulae of fragmentation metrics computed in this study.
Variables Meaning
a
ij
Area (m
2
) of the patch ij. i refers to patch type (class) and j, to the number of patches in the landscape
A Total area of the landscape (m
2
).
n
i
Number of patches of the habitat type (class) i in the landscape
e
ik
Total length of edge (m) in the landscape between patch types i and k
h
ijr
Distance between the cell ijr (located inside the patch ij) and the centroid of patch ij, based on cell centre-to-cell centre distance
z Number of cells in the patch ij
h
ij
Distance (m) of the patch ij to the nearest patch of the same habitat type, based on edge-to-edge distance and computed from cell centre to cell centre
p
ij
The perimeter of the patch ij, measured in number of cell surfaces
x
ij
Represents the metrics which has been calculated in the formulae of mean, area-weighted mean, standard deviation and coefcient of variation
Table 3
Fragmentation metrics used in this study.
Index How to compute Meaning
Number of patches (NP) NP = n
i
The number of patches (fragments) of the same habitat type
Percentage of landscape
(PLAND)
PLAND P
i

n
j1
aij
A
100 The sum of areas (m
2
) of all patches of the same habitat type, divided by the total area of the
landscape (m
2
), multiplied by 100 to convert to percentage
Edge density (ED) ED

m
k1
eik
A
10000 The sum of all edge lengths (m) that involve the patches of the habitat type considered, divided
by the total area of the landscape (m
2
), multiplied by 10,000 to convert to hectares
Patch area coefcient of
variation (AREA_CV)
AREA a
ij
1
10000
_ _
; CV
SD
MN
100 AREA is the area of the patch (m
2
), divided by 10,000 to convert to hectares. CV is the
coefcient of variation
Shape index area-weighted
mean (SHAPE_AM)
SHAPE
p
ij
minp
ij
; AM

n
j1
x
ij
aij

n
j1
aij
_ _ _ _
The area-weighted mean of the shape index
Shape index standard
deviation (SHAPE_SD)
SHAPE
p
ij
minp
ij
; SD

n
j1
xij

n
j1
x
ij
n
i
_ _ _ _
2
ni

_
The standard deviation of the shape index. Represents a measure of variation of the patch
shapes in the landscape in relation to a mean shape
Radius of gyration area-
weighted mean
(GYRATE_AM)

z
r1
hijr
z
; AM

n
j1
x
ij
aij

n
j1
aij
_ _ _ _
Radius of gyration is the mean distance (m) between each patch cell and the centroid of the
patch. Larger values indicate larger patches. It represents a measure of landscape connectivity.
Area-weighted mean is the sum of values of radius of gyration of all patches of the same
habitat type, multiplied by the proportional abundance of the patch (i.e., patch area (m
2
)
divided by the sum of patch areas)
Mean Euclidean nearest
neighbour distance
(ENN_MN)
ENN h
ij
; MN

n
j1
xij
ni
The distance (m) to the nearest patch of same type of habitat, based on the edge-to-edge
distance. Mean is the sum of the values of the distance between all patches of same habitat
type, divided by the number of patches of this habitat type
F.M.V. Carvalho et al. / Biological Conservation 142 (2009) 13921403 1395
(ENN_MN) showed no signicant differences among any of the
landscapes (Fig. 4d).
The landscape remnant vegetation varied according to the slope
(Fig. 5a). The positive relation between these variables can not be
explained by chance only (R
2
= 0.185; p < 0.001). The mean slope
for landscapes dominated by natural vegetation was larger and sta-
tistically different from mean values found in pasture and cropland
areas (inference by condence interval, Fig. 5b). This was also the
case in pasture-dominated landscapes when compared to cropland
areas (Fig. 5b). These results show that preserved areas tend to be
associated to more rugged terrains, while crop-dominated areas
are mostly located in at regions.
The analysis of the landscape metrics with respect to total hab-
itat remaining allows clarifying the inter-relationship between
habitat loss and habitat fragmentation in each land cover type.
There is a clear distinction between cropland fragmentation and
the other land cover units (Fig. 6). All but the mosaic of cropland
and cattle raising landscapes present signicant negative relations
between NP and the proportion of natural vegetation remaining.
However, cropland showed the largest effect, with an increase of
nearly ve fragments for the loss of each 1% of total habitat, sup-
porting the conclusion of its higher fragmentation level. It is also
noted that croplands present lower values of total natural vegeta-
tion remaining.
The results of edge density also support the inter-relationship
between habitat loss and habitat fragmentation, but showed a
more complex relation to land cover categories. In cases that in-
cluded crops (cropland itself and mosaic croplandpasture) there
was a strong positive relation between edge density and total hab-
itat remaining. A positive relation is also observed for pasture
(Fig. 7). The general relation of these variables, regardless of land
cover categories, seems mostly non-linear, with positive relations
occurring for lower values of remaining habitat and negative or
no relation at all observed at higher levels of habitat conservation.
The analysis of fragment sizes in each landscape in relation to
the home range sizes of mammals showed that landscapes domi-
nated by cerrado, and landscapes classied in any intermediate
category which include cerrado had the highest conservation value
for the selected species. Landscapes dominated by crops showed
the smaller number of fragments to maintain these species
(Fig. 8). S. venaticus, P. onca and C. brachyurus are the three species
with greater home ranges, and fragments with sizes ten times
greater than these home ranges were observed only in landscapes
dominated by cerrado and by pasture. For L. colocolo, M. tridactyla
and P. maximus, landscapes with intermediate categories which in-
clude cropland and cerrado (as ccr and ccrp) presented a num-
ber of fragments greater than the other categories, even when
compared with landscapes dominated by cerrado (Fig. 8).
4. Discussion
4.1. Cerrado fragmentation: causes of differences
Land occupation for crops, especially in the southern region of
Gois, occurred initially in areas with better soil fertility. Neverthe-
less, as agricultural technology developed, topography became the
most important feature limiting agriculture. About 95% of areas
with agricultural activities in Gois are located in regions with at
Fig. 2. Grid of Gois State, with 0.5 latitude 0.5 longitude landscape resolution, classied according to dominant cover. c: cerrado; ccr: cerradocropland; ccrp:
cerradocroplandpasture; cp: cerradopasture; cr: cropland;.crp: croplandpasture; p: pasture; uac: urban areacerrado.
1396 F.M.V. Carvalho et al. / Biological Conservation 142 (2009) 13921403
most 4 of slope (Miziara and Ferreira, 2006). If crops were devel-
oped primarily in more at areas, sloping areas are preferably left
as part of the set-aside provision of Brazils 1965 Forest Code, that
requires rural landowners in the Cerrado to keep one-fth of their
lands as Legal Reserve. If this is correct, then fragments of Cerrado
remnant vegetation should be a non-random sample of topography
of the region, and have been located mainly in areas with greater
slopes. This hypothesis was conrmed by the positive relation be-
tween cerrado-dominated landscapes and slope. Brannstrom et al.
(2008) also found that observed differences in the fragmentation
pattern could be due to topography, land tenure and vegetation
dynamics. In both areas, Cerrado remnants occur in pixels with
higher slopes than for agro-pastoral areas.
The distribution pattern of many important elements of biodi-
versity, from which we emphasize plants and birds, are strongly af-
fected by topography and altitude. For example, some groups of
birds tend to occur preferably in ravines with steeper slope (Ribon
et al., 2003), and some group of palms tend to occur in at areas
(Kahn et al., 1988). Therefore, a topography-biased fragmentation
in Cerrado leads to a biased sample of biodiversity.
There was no difference in edge density between crop and pas-
turedominated landscapes. However, crop areas had a large num-
ber of patches than pasture areas, in a same total habitat area. This
result suggests that pasture-dominated landscapes should have
more irregular patches, which have more edge than patches of
more simpler shapes, and this was conrmed by the differences
observed in the shape metrics. Many cropland areas are related
to soya and sugarcane, which are intensely mechanized cultures
(Ratter et al., 1997; Fearnside, 2001). It is possible that in these
more mechanized systems, fragments edges can be more regular
and reect the intensive land use in the region.
A feature that differentiates crops from pasture is that the for-
mer needs a greater infrastructure to distribute the production.
Historically, agricultural areas in Gois increased following the
consolidation of transport infrastructure. Thus, croplands tend to
be located around roads of great circulation (Miziara and Ferreira,
2006). On the other hand, the denser road network found in the
more prominent crop regions induces a more severe fragmenta-
tion, which, as demonstrated by Goosem (1997), may have a great-
er impact on biodiversity.
Colonisation and development of agricultural technology in
Gois occurred primarily in southern regions, closer to centres of
economic growth of the country, and followed a direction towards
Amazonia (Miziara and Ferreira, 2006). Thus, the northeast of Goi-
s suffers a low colonisation pressure due to its geographic position,
but also due to other constraints such as elevation, slope, and
nutrient-poor soils (Sano et al., 2006), which inhibit agricultural
activities. Considering both the current level of preservation and
the smaller risks they face due to the colonisation axis, the north-
eastern areas should be considered as priority areas for the preser-
vation of biodiversity and for the establishment of strategies for
creation of conservation units. However, a clear warning must be
considered that this region had a biased representation of the over-
all Cerrado ora and fauna, and, at least, deserves better biodiver-
sity inventories to evaluate its representativeness.
4.2. Consequences of fragmentation for biodiversity conservation in
landscapes dominated by human activities
Fragmentation has two immediate consequences (Saunders
et al., 1991; Fahrig, 2003): reduction of habitat area and isolation
of remnant habitat patches. Isolation has an effect on population
dominant cover
0
20
40
60
80
100
120
140
160
180
200
220
240
N
P
F
6,109
=23.340, p<0.001
a
a
a
b
c
ab
ab
c c-p p cr-p cr c-cr c-cr-p
c c-p p cr-p cr c-cr c-cr-p
c c-p p cr-p cr c-cr c-cr-p
dominant cover
-10
0
10
20
30
40
50
60
70
P
L
A
N
D
F
6,109
=14.192, p<0.001
bc
a
abc
c
c
b
ab
dominant cover
2.5
3.0
3.5
4.0
4.5
5.0
5.5
6.0
E
D
a
ab
ab
ab
ab ab
b
F
6,109
=2.0619, p=0.063
c c-p p cr-p cr c-cr c-cr-p
dominant cover
100
200
300
400
500
600
700
800
A
R
E
A
_
C
V
F
6,109
=1.8340, p=0.099
a
b
d
c
Fig. 3. Fragmentation metrics at the class level for area, density and edge. (a) NP, number of patches; (b) PLAND, percentage of landscape; (c) ED, edge density and (d)
AREA_CV, patch area coefcient of variation. Different letters at the side of the bars represent statistically different values; same letters represent statistically same values in
Tukey test a posteriori. Dominant cover: c, cerrado; cp, cerradopasture; p, pasture; crp, croplandpasture; cr, cropland; ccr, cerradocropland; ccrp, cerradocropland
pasture.
F.M.V. Carvalho et al. / Biological Conservation 142 (2009) 13921403 1397
viability, as it causes a discontinuity in species distribution pat-
terns, affecting the dynamics and genetic structure of population
in the fragments (Sih et al., 2000).
Fragmentation produces a matrix of habitat different from the
original habitat around the fragments; this matrix, however, is
not necessarily a hostile habitat for all species. The habitat type
of the matrix that surrounds the fragments can facilitate or prevent
movements of individuals among the patches (Gascon et al., 1999;
Joly et al., 2001; Jules and Shahani, 2003; Antongiovanni and Metz-
ger, 2005). Thus, the matrix acts as a lter for dispersal, not as an
impeditive barrier (Ricketts, 2001; Perfecto and Vandermeer,
2002; Pardini, 2004). The capacity of movements of individuals
among fragments also depends on the characteristics of the spe-
cies, as well as the time of isolation, the distance between adjacent
fragments and the degree of connectivity between them (Saunders
et al., 1991; Fahrig and Merriam, 1994; Banks et al., 2005; Ewers
and Didham, 2006). So, population persistence into the fragments
also depends upon the type of matrix in which these fragments
are embedded. The observed differences in pasture and cropland-
dominated landscapes can, therefore, strongly affect the species
that live in remnant fragments.
Fragments with size greater than ten times the home ranges of
S. venaticus, P. onca and C. brachyurus are rare, even in landscapes
dominated by the original vegetation. The results for all species
c c-p p cr-p cr c-cr c-cr-p
dominant cover
1.0
1.5
2.0
2.5
3.0
3.5
4.0
4.5
5.0
5.5
6.0
6.5
S
H
A
P
E
_
A
M
F
6,109
=4.3538, p<0.001
ab
ab
ab
b
b
a
a
c c-p p cr-p cr c-cr c-cr-p
dominant cover
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
1.0
1.1
1.2
S
H
A
P
E
_
S
D
F
6,109
=4.3875, p<0.001
a
ab
ab
b
b
a a
c c-p p cr-p cr c-cr c-cr-p
dominant cover
-2000
0
2000
4000
6000
8000
10000
12000
14000
16000
18000
20000
G
Y
R
A
T
E
_
A
M
F
6,109
=10.334, p<0.001
c
bc
abc
a
c
b
ab
c c-p p cr-p cr c-cr c-cr-p
dominant cover
800
900
1000
1100
1200
1300
1400
1500
1600
1700
1800
E
N
N
_
M
N
F
6,109
=0.46228, p=0.835
a
c
b
d
Fig. 4. Fragmentation metrics at the class level for shape, connectivity and isolation. (a) SHAPE_AM, shape index area-weighted mean; (b) SHAPE_SD, shape index standard
deviation; (c) GYRATE_AM, radius of gyration area-weighted mean and (d) ENN_MN, mean Euclidean nearest neighbour distance. Different letters at the side of the bars
represent statistically different values; same letters represent statistically same values in Tukey test a posteriori. Dominant cover: c, cerrado; cp, cerradopasture; p, pasture;
crp, croplandpasture; cr, cropland; ccr, cerradocropland; ccrp, cerradocroplandpasture.
0 40 80 120 160 200 240
mean slope
0
20
40
60
80
100
P
L
A
N
D
r
2
=0.1818; p<0.001
c c-p p cr-p cr c-cr c-cr-p
dominant cover
0
20
40
60
80
100
120
M
e
a
n

s
l
o
p
e
a
b
Fig. 5. Relation between (a) mean slope and percentage of Cerrado vegetation remnants in Gois State and (b) between mean slope with cover type and land use in Gois
State.
1398 F.M.V. Carvalho et al. / Biological Conservation 142 (2009) 13921403
analysed also suggest that landscapes dominated by crops are
more damaging to the survival of mammal species. However, even
in these landscapes it is still possible to nd fragments of natural
vegetation within the criterion analysed. Thus, this analysis shows
that fragments capable to support populations of the species are
still present, but they need a planned action to restore their conser-
vation value for biodiversity.
Reduction of habitat area due to fragmentation can lead to a de-
crease in species richness and population size, increasing extinc-
tion probabilities especially for larger species (Wilcox and
Murphy, 1985; Saunders et al., 1991; Fahrig and Merriam, 1994;
Tilman et al., 1994; Brooks et al., 2002). Our analysis showed that
this could be true for S. venaticus, P. onca and C. brachyurus mainly
in crop-dominated areas. The fragmentation pattern observed sug-
gests that, compared to crops, pasture areas could favour conserva-
tion of larger species, and also allows higher species richness in
fragments. However, fragments in pasture areas are also more
irregular, what can cause an increase of edges and loss of core area.
A fragment of irregular shape may suffer more edge effects related
to abiotic alterations, due to the increase in wind and light, the de-
crease in soil moisture, and changes in nutrient ow (Saunders
et al., 1991; Murcia, 1995). These changes affect the biotic commu-
nity, and can lead to tree falls and the loss and substitution of spe-
cies (fragment edges can be invaded by species from the matrix, or
species typical from edges). Extension of edge effects is variable,
and smaller and more irregular fragments are more affected, as
these effects can reach almost all of the fragment area (Murcia,
1995; Parker et al., 2005). Invasive plants, traditionally related to
edge effects (e.g. introduction of molassa [Melinis minutiora]),
are also considered one of the major threats of Cerrado, especially
due to its relation to re frequency and intensity (Klink and Mach-
ado, 2005). The Cerrado, however, is formed by a set of different
phyto-physiognomies, including several forms of open vegetation,
which receive the natural inuence of other systems around. It is
N
P
PLAND
0 20 40 60 80 100
0
40
80
120
160
200
240
280
cerrado
PLAND
N
P
0 20 40 60 80 100
0
40
80
120
160
200
240
280
cropland
PLAND
N
P
0 20 40 60 80 100
0
40
80
120
160
200
240
280
cropland-pasture
PLAND
N
P
0 20 40 60 80 100
0
40
80
120
160
200
240
280
pasture
PLAND
N
P
0 20 40 60 80 100
0
40
80
120
160
200
240
280
cerrado-pasture
0 20 40 60 80 100
PLAND
0
40
80
120
160
200
240
280
N
P
a
c
e
f
b
d
Fig. 6. Relation between percentage of remnant vegetation in the landscape and number of patches, for the categories: cerrado (c), cropland (cr), croplandpasture (crp),
pasture (p) and cerradopasture (cp). Regression line equations: c: NP = 99.921 1.107 PLAND; cr: NP = 260.131 5.221 PLAND; crp: NP = 113.867 + 0.306 PLAND; p:
NP = 93.147 0.843 PLAND; cp: NP = 108.662 1.192 PLAND; total: NP = 143.5992 1.8192 PLAND.
F.M.V. Carvalho et al. / Biological Conservation 142 (2009) 13921403 1399
possible that vegetation and fauna of these systems have a long
evolutionary history with this kind of alterations and classical edge
effect does not apply here. Finally, we can conservatively consider
that fragment size is a more important feature than shape for pres-
ervation of species in this system.
It is important to note that studies of fragmentation patterns
using quantitative metrics can lead to different results if different
scales are used (Tischendorf, 2001; Saura, 2002; Millington et al.,
2003; Buyantuyev and Wu, 2007). Some macroecological studies
of vertebrate species richness patterns in the Cerrado biome use
cells of 1 longitude 1 latitude, mainly due to scarce information
on biodiversity distribution and the availability of some general
distribution maps at a large scale (Diniz-Filho and SantAna,
1998; Diniz-Filho et al., 2006, 2007). This macroecological or con-
servation biogeography approach (Whittaker et al., 2005) can pro-
vide overall guidelines for conservation and dene the focus for
more local and effective conservation efforts. Thus, these studies
can be considered as a starting point for more detailed strategies
at a local scale. In the present study, we used a slightly lower scale
(0.5 latitude 0.5 longitude) to balance between the analysis of
the conservation perspective of a large area and the use the frag-
mentation pattern as a surrogate for biodiversity. The set of met-
rics used here was appropriate to assess fragmentation patterns
in Cerrado and highlighted important differences in land use for
croplands and for pasture in Gois, which can have important con-
sequences for Cerrado biodiversity.
Fragmentation of the Cerrado biome is an ongoing process. In
particular, the conversion of more traditional land uses to biofuel
production is imminent. Biofuels, like biodiesel or ethanol, are
alternatives to petroleum as energy source, presenting a market
in expansion and a large pressure for the establishment of new
areas for production of its raw material, mainly soya, castor beans
and other oil-bearing plants, and specially sugarcane in Brazilian
Cerrado (Koh, 2007; Koh and Ghazoul, 2008; Fargione et al.,
2008). This increase represents a great potential to habitat and
biodiversity losses, increasing pressure on preserved natural
PLAND
E
D
0 20 40 60 80 100
-1
0
1
2
3
4
5
6
7
cerrado
PLAND
E
D
0 20 40 60 80 100
-1
0
1
2
3
4
5
6
7
cropland
PLAND
E
D
0 20 40 60 80 100
-1
0
1
2
3
4
5
6
7
cropland-pasture
PLAND
E
D
0 20 40 60 80 100
-1
0
1
2
3
4
5
6
7
pasture
PLAND
E
D
0 20 40 60 80 100
-1
0
1
2
3
4
5
6
7
cerrado-pasture
0 20 40 60 80 100
PLAND
0
1
2
3
4
5
6
7
E
D
a
c
e
f
b
d
Fig. 7. Relation between percentage of remnant vegetation in the landscape and edge density, for the categories: cerrado (c), cropland (cr), croplandpasture (crp), pasture
(p) and cerradopasture (cp). Regression line equations: c: ED = 5.932 0.0342 PLAND; cr: ED = 2.581 + 0.12 PLAND; crp: ED = 1.627 + 0.133 PLAND; p:
ED = 3.211 + 0.044 PLAND; cp: ED = 5.519 0.015 PLAND; total: ED = 1.73 + 0.156 PLAND 0.0017 PLAND^2.
1400 F.M.V. Carvalho et al. / Biological Conservation 142 (2009) 13921403
areas, with unpredictable consequences (Koh, 2007). Current
expectations are that sugarcane will occupy sites previously occu-
pied by pastures, and may increase the fragmentation of those
areas, if it follows the general patterns presented by croplands
in this study.
Ecosystem services are processes and conditions by which eco-
systems provide benets for humans (Costanza et al., 1997). These
services include climate regulation, water and food supply, control
of drought and ood, maintenance of biodiversity and recreation
(Prato, 2007; Li et al., 2007). Landscape changes caused by human
activities may disrupt those services through habitat loss and
extinction of species and ecological interactions. The general pat-
tern of distribution of habitat remnants and the size of those
patches support the view that in areas dominated by cropland
activities, the purpose of fragment conservation is mainly related
to their potential for maintenance of ecosystem services. Other-
wise, landscapes dominated by pastures and those that maintain
original vegetation (e.g. the northeastern area of Gois) should be
considered the areas with higher direct biodiversity conservation
value. Thus, these different approaches represent a concentration
of conservation efforts on ecological interactions that could affect
production (e.g. insect pollination) in cropland-dominated areas,
and establishment conservation units or biodiversity corridors in
pasture-dominated areas.
5. Conclusion
This study showed that landscapes dominated by crops are
more fragmented than those dominated by pasture. Concerning
biodiversity conservation, land use for cropland activities produce
higher fragmentation levels than pasture activities. Remnant vege-
tation area is similar in both landscapes. Nevertheless, the frag-
ments of pasture areas were more irregular. The distribution of
land use types are strongly affected by topography, leading to a
biased distribution of remnant fragments in relation to slope. Gen-
c c-p p cr-p cr c-cr c-cr-p
dominant cover
0.0
0.5
1.0
1.5
2.0
2.5
3.0
3.5
N
u
m
b
e
r

o
f

f
r
a
g
m
e
n
t
s
c c-p p cr-p cr c-cr c-cr-p
dominant cover
0.0
0.5
1.0
1.5
2.0
2.5
3.0
3.5
N
u
m
b
e
r

o
f

f
r
a
g
m
e
n
t
s
c c-p p cr-p cr c-cr c-cr-p
dominant cover
0.0
0.5
1.0
1.5
2.0
2.5
3.0
3.5
N
u
m
b
e
r

o
f

f
r
a
g
m
e
n
t
s
c c-p p cr-p cr c-cr c-cr-p
dominant cover
0.0
0.5
1.0
1.5
2.0
2.5
3.0
3.5
N
u
m
b
e
r

o
f

f
r
a
g
m
e
n
t
s
c c-p p cr-p cr c-cr c-cr-p
dominant cover
0.0
0.5
1.0
1.5
2.0
2.5
3.0
3.5
N
u
m
b
e
r

o
f

f
r
a
g
m
e
n
t
s
c c-p p cr-p cr c-cr c-cr-p
dominant cover
0.0
0.5
1.0
1.5
2.0
2.5
3.0
3.5
N
u
m
b
e
r

o
f

f
r
a
g
m
e
n
t
s
a
c
e
f
d
b
Fig. 8. Number of fragments with area greater than 10 times the home range of mammal species in landscapes of Gois State. (a) Bush dog, Speothos venaticus; (b) pampas cat,
Leopardus colocolo; (c) jaguar, Panthera onca; (d) giant anteater, Myrmecophaga tridactyla; (e) giant armadillo, Priodontes maximus and (f) maned-wolf, Chrysocyon brachyurus.
F.M.V. Carvalho et al. / Biological Conservation 142 (2009) 13921403 1401
eral landscape patterns support the need of different approaches
for crop and pasture-dominated systems.
Acknowledgments
We thank three anonymous reviewers for very useful critiques
and comments of the manuscript. This work was partially funded
by the Brazilian Ministry of Science and Technology Research
Council (MCT CNPq) through Grants given to PDM and LGF.
References
Andrn, H., 1994. Effects of habitat fragmentation on birds and mammals in
landscapes with different proportions of suitable habitat: a review. Oikos 71,
355366.
Antongiovanni, M., Metzger, J.P., 2005. Inuence of matrix habitats on the
occurrence of insectivorous bird species in Amazonian forest fragments.
Biological Conservation 122, 441451.
Baldi, G., Guerschman, J.P., Paruelo, J.M., 2006. Characterizing fragmentation in
temperate South America grasslands. Agriculture Ecosystems & Environment
116, 197208.
Banks, S.C., Finlayson, G.R., Lawson, S.J., Lindenmayer, D.B., Paetkau, D., Ward, S.J.,
Taylor, A.C., 2005. The effects of habitat fragmentation due to forestry
plantation establishment on the demography and genetic variation of a
marsupial carnivore, Antechinus agilis. Biological Conservation 122, 581597.
Bennett, A.F., Radford, J.Q., Haslem, A., 2006. Properties of land mosaics:
implications for nature conservation in agricultural environments. Biological
Conservation 133, 250264.
Brannstrom, C., Jepson, W., Filippi, A.M., Redo, D., Xu, Z.W., Ganesh, S., 2008. Land
change in the Brazilian Savanna (Cerrado), 19862002: comparative analysis
and implications for land-use policy. Land Use Policy 25, 579595.
Brooks, T.M., Mittermeier, R.A., Mittermeier, C.G., Fonseca, G.A.B., Rylands, A.B.,
Konstant, W.R., Flick, P., Pilgrim, J., Oldeld, S., Magin, G., Hilton-Taylor, C., 2002.
Habitat loss and extinction in the hotspots of biodiversity. Conservation Biology
16, 909923.
Burel, F., Butet, A., Delettre, Y.R., de la Pena, N.M., 2004. Differential response of
selected taxa to landscape context and agricultural intensication. Landscape
and Urban Planning 67, 195204.
Buyantuyev, A., Wu, J.G., 2007. Effects of thematic resolution on landscape pattern
analysis. Landscape Ecology 22, 713.
Cardillo, M., Mace, G.M., Jones, K.E., Bielby, J., Bininda-Emonds, O.R.P., Sechrest, W.,
Orme, C.D.L., Purvis, A., 2005. Multiple causes of high extinction risk in large
mammal species. Science 309, 12391241.
Cheida, C.C., Nakano-Oliveira, E., Fusco-Costa, R., Rocha-Mendes, F., Quadros, J.,
2006. Ordem Carnivora. In: Reis, N.R., Peracchi, A.L., Pedro, W.A., Lima, I.P. (Eds.).
Mamferos do Brasil. Editora UEL, Londrina, pp. 231276.
Colli, G.R., Bastos, R.P., Arajo, A.B., 2002. The character and dynamics of the Cerrado
herpetofauna. In: Oliveira, P.S., Marquis, R.J. (Eds.), The Cerrrados of Brazil:
Ecology and Natural History of a Neotropical Savanna. Columbia University
Press, New York, pp. 223241.
Costanza, R., dArge, R., de Groot, R., Farber, S., Grasso, M., Hannon, B., Limburg, K.,
Naeem, S., ONeill, R.V., Paruelo, J., Raskin, R.G., Sutton, P., van den Belt, M., 1997.
The value of the worlds ecosystem services and natural capital. Nature 387,
253260.
Damuth, J., 1981. Population density and body size in mammals. Nature 290, 699
700.
DeMatteo, K.E., Loiselle, B.A., 2008. New data on the status and distribution of the
bush dog (Speothos venaticus): evaluating its quality of protection and directing
research efforts. Biological Conservation 141, 24942505.
Dijak, W.D., Thompson, F.R., 2000. Landscape and edge effects on the distribution of
mammalian predators in Missouri. Journal of Wildlife Management 64, 209
216.
Diniz-Filho, J.A.F., SantAna, C.E.R., 1998. Macroecological analysis of South America
owls (Strigiformes) using philogenetic independent contrasts. Journal of
Comparative Biology 3, 2732.
Diniz-Filho, J.A.F., Bini, L.M., Pinto, M.P., Rangel, T.F.L.V., Carvalho, P., Bastos, R.P.,
2006. Anuran species richness, complementarity and conservation conicts in
Brazilian Cerrado. Acta OecologicaInternational Journal of Ecology 29, 915.
Diniz-Filho, J.A.F., Bini, L.M., Pinto, M.P., Rangel, T.F.L.V., Carvalho, P., Vieira, S.L.,
Bastos, R.P., 2007. Conservation biogeography of anurans in Brazilian Cerrado.
Biodiversity and Conservation 16, 9971008.
Eiten, G., 1982. Brazilian savannas. In: Huntley, B.J., Walker, B.H. (Eds.), Ecological
Studies, Ecology of Tropical Savannas, vol. 42. Springer-Verlag, New York, pp.
2547.
Ewers, R.M., Didham, R.K., 2006. Confounding factors in the detection of species
responses to habitat fragmentation. Biological Reviews 81, 117142.
Fagan, W.F., Holmes, E.E., 2006. Quantifying the extinction vortex. Ecology Letters 9,
5160.
Fahrig, L., 2003. Effects of habitat fragmentation on biodiversity. Annual Review of
Ecology and Systematics 34, 487515.
Fahrig, L., Merriam, G., 1994. Conservation of fragmented populations. Conservation
Biology 8, 5059.
Fargione, J., Hill, J., Tilman, D., Polasky, S., Hawthorne, P., 2008. Land clearing and the
biofuel carbon debt. Science 319, 12351238.
Fearnside, P.M., 2001. Soybean cultivation as a threat to the environment in Brazil.
Environmental Conservation 28, 2338.
Fernandez, M.H., Vrba, E.S., 2005. Body size, biomic specialization and range size of
African large mammals. Journal of Biogeography 32, 12431256.
Gascon, C., Lovejoy, T.E., Bierregaard, R.O., Malcolm, J.R., Stouffer, P.C., Vasconcelos,
H.L., Laurance, W.F., Zimmerman, B., Tocher, M., Borges, S., 1999. Matrix habitat
and species richness in tropical forest remnants. Biological Conservation 91,
223229.
Gautam, A.P., Webb, E.L., Shivakoti, G.P., Zoebisch, M.A., 2003. Land use dynamics
and landscape change pattern in a mountain watershed in Nepal. Agriculture
Ecosystems & Environment 99, 8396.
Goosem, M., 1997. Internal fragmentation: the effects of roads, highway, and
powerline clearings on movements and mortality of rainforest vertebrates. In:
Laurance, W.F., Bierregaard, R.O., Jr. (Eds.), Tropical forest remnants: ecology,
Management, and Conservation of Fragmented Communities. The University of
Chicago Press, Chicago and London, pp. 241255.
Grau, H.R., Gasparri, N.I., Aide, T.M., 2005. Agriculture expansion and deforestation
in seasonally dry forests of northwest Argentina. Environmental Conservation
32, 140148.
Gustafson, E.J., 1998. Quantifying landscape spatial pattern: what is the state of the
art? Ecosystems 1, 143156.
Hargis, C.D., Bissonette, J.A., David, J.L., 1998. The behavior of landscape metrics
commonly used in the study of habitat fragmentation. Landscape Ecology 13,
167186.
IBAMA, 2003. Lista nacional das espcies da fauna Brasileira ameaadas de extino.
<www.meioambiente.gov.br/port/sbf/fauna/ordem4o.html> (accessed
10.10.2007).
IBGE, 2004. Mapa de biomas do Brasil. Escala 1:5.000.000. <http://
mapas.ibge.gov.br/biomas2/viewer.htm> (accessed 10.2.2007).
Jetz, W., Carbone, C., Fulford, J., Brown, J.H., 2004. The scaling of animal space use.
Science 306, 266268.
Joly, P., Miaud, C., Lehmann, A., Grolet, O., 2001. Habitat matrix effects on pond
occupancy in newts. Conservation Biology 15, 239248.
Jules, E.S., Shahani, P., 2003. A broader ecological context to habitat fragmentation:
why matrix habitat is more important than we thought. Journal of Vegetation
Science 14, 459464.
Kahn, F., Mejia, K., Castro, A., 1988. Species richness and density of palms in terra
rme forests of Amazonia. Biotropica 20, 266269.
Kelt, D.A., Van Vuren, D., 1999. Energetic constraints and the relationship between
body size and home range area in mammals. Ecology 80, 337340.
Kirk, D.A., Bathe, G.M., 1994. Population size and home range of black-naped hares
Lepus nigricollis nigricollis on Cousin Island (Seychelles, Indian Ocean).
Mammalia 58, 557562.
Klink, C.A., Machado, R.B., 2005. Conservation of the Brazilian Cerrado. Conservation
Biology 19, 707713.
Klink, C.A., Moreira, A.G., 2002. Past and current human occupation, and land use.
In: Oliveira, P.S., Marquis, R.J. (Eds.), The Cerrados of Brazil: Ecology and Natural
History of a Neotropical Savanna. Columbia University Press, New York, pp. 69
88.
Koh, L.P., 2007. Potential habitat and biodiversity losses from intensied biodiesel
feedstock production. Conservation Biology 21, 13731375.
Koh, L.P., Ghazoul, J., 2008. Biofuels, biodiversity, and people: understanding
the conicts and nding opportunities. Biological Conservation 141, 2450
2460.
Kuper, W., Sommer, J.H., Lovett, J.C., Barthlott, W., 2006. Deciency in African plant
distribution data missing pieces of the puzzle. Botanical Journal of the Linnean
Society 150, 355368.
Laidlaw, R.K., 2000. Effects of habitat disturbance and protected areas on mammals
of peninsular Malaysia. Conservation Biology 14, 16391648.
Li, R.Q., Dong, M., Cui, J.Y., Zhang, L.L., Cui, Q.G., He, W.M., 2007. Quantication of the
impact of land-use changes on ecosystem services: a case study in Pingbian
County, China. Environmental Monitoring and Assessment 128, 503510.
MacDonald, D.W., Rushton, S., 2003. Modelling space use and dispersal of mammals
in real landscapes: a tool for conservation. Journal of Biogeography 30, 607
620.
Machado, R.B., Ramos Neto, M.B., Pereira, P., Caldas, E., Gonalves, D., Santos, N.,
Tabor, K., Steininger, M., 2004. Estimativas de perda da rea do Cerrado
brasileiro. Conservation International, Brasilia.
McGarigal, K., Marks, B.J., 1995. FRAGSTATS: spatial pattern analysis program for
quantifying landscape structure., USDA For. Serv. Gen. Tech. Rep.
Metzger, J.P., 1999. Estrutura da paisagem e fragmentao: anlise bibliogrca.
Anais da Academia Brasileira de Cincias 71, 435463.
Metzger, J.P., 2003. Estrutura da paisagem: o uso adequado de mtricas. In: Cullen,
L., Jr., Rudran, R., Valladares-Padua, C. (Eds.), Mtodos de Estudos em Biologia da
Conservao e Manejo da Vida Silvestre. Universidade Federal do Paran,
Curitiba, pp. 423453.
Millington, A.C., Velez-Liendo, X.M., Bradley, A.V., 2003. Scale dependency in
multitemporal mapping of forest fragmentation in Bolivia: implications for
explaining temporal trends in landscape ecology and applications to
biodiversity conservation. Isprs Journal of Photogrammetry and Remote
Sensing 57, 289299.
Miranda, G.H.B., 2004. Ecologia e Conservao do Tamandu-Bandeira
(Myrmecophaga tridactyla, Linnaeus, 1758) no Parque Nacional das Emas. PhD
thesis, Universidade de Braslia, 81 pp.
1402 F.M.V. Carvalho et al. / Biological Conservation 142 (2009) 13921403
Miziara, F., Ferreira, N.C., 2006. Expanso da fronteira agrcola e evoluo da
ocupao e uso do espao no Estado de Gois: subsdios poltica ambiental. In:
Ferreira, L.G. (Ed.), Conservao da Biodiversidade e Sustentabilidade Ambiental
em Gois: Prioridades. Estratgias e Perspectivas. Ed. Canone, Goinia, pp. 94
109.
Murcia, C., 1995. Edge effects in fragmented forests: implications for conservation.
Trends in Ecology & Evolution 10, 5862.
Myers, N., Mittermeier, R.A., Mittermeier, C.G., Fonseca, G.A.B., Kent, J., 2000.
Biodiversity hotspots for conservation priorities. Nature 403, 853858.
Nelson, B.W., Ferreira, C.A.C., Dasilva, M.F., Kawasaki, M.L., 1990. Endemism Centers,
Refugia and Botanical Collection Density in Brazilian Amazonia. Nature 345,
714716.
OGrady, J.J., Reed, D.H., Brook, B.W., Frankham, R., 2004. What are the best
correlates of predicted extinction risk? Biological Conservation 118, 513520.
Oliveira, T.G., Tortato, M.A., Silveira, L., Kasper, C.B., Mazim, F.D., Jcomo, A.T.A.,
Lucherini, M., Soares, J.B.G., Marques, R.V., Sunquist, M., 2008. Ocelot ecology
and its effect on the small-felid guild in the lowland Neotropics. In: Macdonald,
D.W., Loveridge, A. (Eds.), Biology and Conservation of Wild Felids. Oxford
University Press, Oxford.
Pardini, R., 2004. Effects of forest fragmentation on small mammals in an Atlantic
Forest landscape. Biodiversity and Conservation 13, 25672586.
Pardini, R., de Souza, S.M., Braga-Neto, R., Metzger, J.P., 2005. The role of forest
structure, fragment size and corridors in maintaining small mammal
abundance and diversity in an Atlantic forest landscape. Biological
Conservation 124, 253266.
Parker, T.H., Stansberry, B.M., Becker, C.D., Gipson, P.S., 2005. Edge and area effects
on the occurrence of migrant forest songbirds. Conservation Biology 19, 1157
1167.
Parks, S.A., Harcourt, A.H., Tobler, W., Deichmann, U., Gottsegen, J., Maloy, K., 2002.
Reserve size, local human density, and mammalian extinctions in US protected
areas. Conservation Biology 16, 800808.
Perfecto, I., Vandermeer, J., 2002. Quality of agroecological matrix in a tropical
montane landscape: ants in coffee plantations in southern Mexico.
Conservation Biology 16, 174182.
Potts, S.G., Petanidou, T., Roberts, S., OToole, C., Hulbert, A., Willmer, P., 2006. Plant-
pollinator biodiversity and pollination services in a complex Mediterranean
landscape. Biological Conservation 129, 519529.
Prato, T., 2007. Selection and evaluation of projects to conserve ecosystem services.
Ecological Modelling 203, 290296.
Promislow, D.E.L., Harvey, P.H., 1990. Living fast and dying young: a comparative
analysis of life history variation among mammals. Journal of Zoology 220, 417
437.
Ratter, J.A., Ribeiro, J.F., Bridgewater, S., 1997. The Brazilian cerrado vegetation and
threats to its biodiversity. Annals of Botany 80, 223230.
Redford, K.H., Fonseca, G.A.B., 1986. The role of gallery forest in the zoogeography of
the Cerrados non-volant mammalian fauna. Biotropica 18, 126135.
Ribon, R., Simon, J.E., De Mattos, G.T., 2003. Bird extinctions in Atlantic forest
fragments of the Vicosa region, southeastern Brazil. Conservation Biology 17,
18271839.
Ricketts, T.H., 2001. The matrix matters: effective isolation in fragmented
landscapes. American Naturalist 158, 8799.
Riitters, K.H., Oneill, R.V., Hunsaker, C.T., Wickham, J.D., Yankee, D.H., Timmins, S.P.,
Jones, K.B., Jackson, B.L., 1995. A factor-analysis of landscape pattern and
structure metrics. Landscape Ecology 10, 2339.
Sano, E.E., Dambrs, L.A., Oliveira, G.C., 2006. Padres de cobertura de solos do
Estado de Gois. In: Ferreira, L.G. (Ed.), Conservao da Biodiversidade e
Sustentabilidade Ambiental em Gois: Prioridades. Estratgias e Perspectivas.
Ed. Canone, Goinia, pp. 7693.
Sano, E.E., Ferreira, L.G., Asner, G., Steinke, E., 2007. Spatial and temporal
probabilities of obtaining cloud-free Landsat images over the Brazilian
Tropical Savanna. International Journal of Remote Sensing 28, 27392752.
Sano, E.E., Rosa, R., Brito, J.L.S., Ferreira, L.G., 2008. Mapeamento semidetalhado do
uso da terra do Bioma Cerrado. Pesquisa Agropecuaria Brasileira 43, 153156.
Saunders, D.A., Hobbs, R.J., Margules, C.R., 1991. Biological consequences of
ecosystem fragmentation: a review. Conservation Biology 5, 1832.
Saura, S., 2002. Effects of minimum mapping unit on land cover data spatial
conguration and composition. International Journal of Remote Sensing 23,
48534880.
Sih, A., Jonsson, B.G., Luikart, G., 2000. Habitat loss: ecological, evolutionary and
genetic consequences. Trends in Ecology & Evolution 15, 132134.
Silveira, L., 2004. Ecologia Comparada e Conservao da Ona-Pintada (Panthera
onca) e Ona-Parda (Puma concolor) no Cerrado e Pantanal. PhD thesis.
Universidade de Braslia, 240 pp.
Silveira, L., Jcomo, A.T.A., Furtado, M.M., Torres, N.M., Sollmann, R., Vynne, C.,
accepted for publication. Ecology of the giant armadillo (Priodontes maximus) in
the grasslands of Central Brazil. Edentata.
Tilman, D., May, R.M., Lehman, C.L., Nowak, M.A., 1994. Habitat destruction and the
extinction debt. Nature 371, 6566.
Tilman, D., Fargione, J., Wolff, B., DAntonio, C., Dobson, A., Howarth, R., Schindler, D.,
Schlesinger, W.H., Simberloff, D., Swackhamer, D., 2001. Forecasting
agriculturally driven global environmental change. Science 292, 281284.
Tischendorf, L., 2001. Can landscape indices predict ecological processes
consistently? Landscape Ecology 16, 235254.
Tobler, M., Honorio, E., Janovec, J., Reynel, C., 2007. Implications of collection
patterns of botanical specimens on their usefulness for conservation planning:
an example of two neotropical plant families (Moraceae and Myristicaceae) in
Peru. Biodiversity and Conservation 16, 659677.
Torbick, N.M., Qi, J.G., Roloff, G.J., Stevenson, R.J., 2006. Investigating impacts of
land-use land cover change on wetlands in the Muskegon River Watershed,
Michigan, USA. Wetlands 26, 11031113.
Vandermeer, J., Perfecto, I., 2007. The agricultural matrix and a future paradigm for
conservation. Conservation Biology 21, 274277.
Whittaker, R.J., Araujo, M.B., Paul, J., Ladle, R.J., Watson, J.E.M., Willis, K.J., 2005.
Conservation Biogeography: assessment and prospect. Diversity and
Distributions 11, 323.
Wilcox, B.A., Murphy, D.D., 1985. Conservation strategy: the effects of
fragmentation on extinction. The American Naturalist 125, 879887.
Zar, J.H., 1999. Biostatistical Analysis, fourth ed. Prentice-Hall, Englewood Cliffs, NJ.
F.M.V. Carvalho et al. / Biological Conservation 142 (2009) 13921403 1403