Carvalho Et Al. 2009 the Cerrado Into-pieces

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The Cerrado into-pieces: Habitat fragmentation as a function of landscapeuse 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, Brazilb 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 toconservation 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 quantified 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 modifications occurring in the landscape (Burel et al.,

2004).

Habitat fragmentation is often defined 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 definition

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 definition 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 profitable (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 modifications 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: [email protected](P. De Marco).

Biological Conservation 142 (2009) 13921403

Contents lists available at ScienceDirect

Biological Conservation

j o u r n a l h o m e p a g e : w w w . e l s e v i e r . c o m / l o c a t e / b i o c o n
mailto:[email protected]://www.sciencedirect.com/science/journal/00063207http://www.elsevier.com/locate/bioconhttp://www.elsevier.com/locate/bioconhttp://www.sciencedirect.com/science/journal/00063207mailto:[email protected]


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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 aspatially 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 specifically 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 efficient 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. Consideringthe 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 km2, 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 undera 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), althoughMachado 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 identification 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 influence 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 interpretationof 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 shapefile format and visually interpreted

onthe 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 mappingthe 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 significant 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 Identification of Priority

Areas for Biodiversity Conservation in Gois State), which con-

sisted in the interpretation of 23 Landsat scenes, extensive field

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
http://www.edc.usgs.gov/products/elevation/gtopo30/hydro/index.htmlhttp://www.edc.usgs.gov/products/elevation/gtopo30/hydro/index.htmlhttp://www.edc.usgs.gov/products/elevation/gtopo30/hydro/index.htmlhttp://www.edc.usgs.gov/products/elevation/gtopo30/hydro/index.html


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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 km2 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 significantly 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 inTable 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 dominantin each cell. In cases where this criterion did not hold, the cell was

classified 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 configuration 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 defined 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

configuration 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 sufficient 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 significant

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 useand (b)slope (percent rise) andrivers. Percent riseof slope equals100 when slope in degrees equals45 and, as theslope

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


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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 regressionanalysis according toZar (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). Significant difference was ob-

served in ED values only between Cerrado and pasture (Fig. 3c).

There was no significant difference for the patch area coefficient

of variation (AREA_CV) among any of the landscapes (Fig. 3d).

The shape indices, SHAPE_AM e SHAPE_SD, were significantly 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

aij Area (m2) of the patchij.i refers to patch type (class) and j, to the number of patches in the landscape

A Total area of the landscape (m2).

ni Number of patches of the habitat type (class)i in the landscape

eik Total length of edge (m) in the landscape between patch typesi and k

hijr Distance between the cellijr(located inside the patchij) and the centroid of patch ij, based on cell centre-to-cell centre distance

z Number of cells in the patchij

hij Distance (m) of the patchij to the nearest patch of the same habitat type, based on edge-to-edge distance and computed from cell centre to cell centre

pij The perimeter of the patchij, measured in number of cell surfaces

xij Represents the metrics which has been calculated in the formulae of mean, area-weighted mean, standard deviation and coefficient of variation

Table 3

Fragmentation metrics used in this study.

Index How to compute Meaning

Number of patches (NP) NP = ni The number of patches (fragments) of the same habitat type

Percentage of landscape

(PLAND)

PLANDPi

Pnj1

aij

A 100 The sum of areas (m2) of all patches of the same habitat type, divided by the total area of the

landscape (m2), multiplied by 100 to convert to percentage

Edge density (ED) ED

Pmk1

eikA 10000 Thesum of all edge lengths (m)that involve thepatches of thehabitat type considered, divided

by the total area of the landscape (m2), multiplied by 10,000 to convert to hectares

Patch area coefficient of

variation (AREA_CV)

AREAaij 110000

; CV SDMN100 AREA is the area of the patch (m

2), divided by 10,000 to convert to hectares. CV is the

coefficient of variation

Shape index area-weighted

mean (SHAPE_AM)

SHAPE pij

minpij; AM

Pnj1 xij

aijPnj1

aij

The area-weighted mean of the shape index

Shape index standard

deviation (SHAPE_SD)

SHAPE pij

minpij; SD

ffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi ffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi ffiffiffiffiffiPnj1 xij

Pnj1xijni

2ni

vuut 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)

Pzr1

hijrz

; AMPn

j1 xijaijPnj1

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 (m2)

divided by the sum of patch areas)

Mean Euclidean nearest

neighbour distance

(ENN_MN)

ENNhij; MN

Pnj1

xij

niThe 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



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(ENN_MN) showed no significant 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 (R2 = 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 confidence 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 flat regions.

The analysis of the landscape metrics with respect to total hab-

itat remaining allows clarifying the inter-relationship betweenhabitat 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 significant negative relations

between NP and the proportion of natural vegetation remaining.

However, cropland showed the largest effect, with an increase of

nearly five 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) therewas 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 classified 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 andC. brachyurus are the three species

with greater home ranges, and fragments with sizes ten times

greater than these home ranges were observed only in landscapesdominated 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, classified according to dominant cover. c: cerrado; ccr: cerradocropland; ccrp:

cerradocroplandpasture; cp: cerradopasture; cr: cropland;.crp: croplandpasture; p: pasture; uac: urban areacerrado.



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most 4of slope (Miziara and Ferreira, 2006). If crops were devel-

oped primarily in more flat areas, sloping areas are preferably leftas part of the set-aside provision of Brazils 1965 Forest Code, that

requires rural landowners in the Cerrado to keep one-fifth 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 confirmed 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 ofbirds tend to occur preferably in ravines with steeper slope ( Ribon

et al., 2003), and some group of palms tend to occur in flat 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 confirmed 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 regularand reflect 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 agriculturalactivities. 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 flora 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 isolationof remnant habitat patches. Isolation has an effect on population

dominant cover

0

20

40

60

80

100

120

140

160

180

200

220

240

NP

F6,109=23.340, p


7/12

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 filter 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 landscapesdominated 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

2.53.0

3.5

4.0

4.5

5.0

5.5

6.0

6.5

SH

APE

_AM

F6,109=4.3538, p


8/12

analysed also suggest that landscapes dominated by crops are

more damaging to the survival of mammal species. However, evenin these landscapes it is still possible to find 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. oncaandC. brachyurusmainly

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 infragments. 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 relatedto abiotic alterations, due to the increase in wind and light, the de-

crease in soil moisture, and changes in nutrient flow (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 minutiflora]),

are also considered one of the major threats of Cerrado, especially

due to its relation to fire 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 influence of other systems around. It is

NP

PLAND

0 20 40 60 80 1000

40

80

120

160

200

240

280cerrado

PLAND

NP

0 20 40 60 80 1000

40

80

120

160

200

240

280

cropland

PLAND

NP

0 20 40 60 80 1000

40

80

120

160

200

240

280cropland-pasture

PLAND

NP

0 20 40 60 80 1000

40

80

120

160

200

240

280

pasture

PLAND

N

P

0 20 40 60 80 1000

40

80

120

160

200

240

280

cerrado-pasture

0 20 40 60 80 100

PLAND

0

40

80

120

160

200

240

280

NP

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 = 99.9211.107 PLAND;cr: NP = 260.1315.221 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.



9/12

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 considerthat 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 1longitude 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 define 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

(0.5latitude 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

ED

0 20 40 60 80 100-1

0

1

2

3

4

5

6

7cerrado

PLAND

ED

0 20 40 60 80 100-1

0

1

2

3

4

5

6

7

cropland

PLAND

ED

0 20 40 60 80 100-1

0

1

2

3

4

5

6

7

cropland-pasture

PLAND

ED

0 20 40 60 80 100-1

0

1

2

3

4

5

6

7

pasture

PLAND

ED

0 20 40 60 80 100-1

0

12

3

4

5

6

7

cerrado-pasture

0 20 40 60 80 100

PLAND

0

1

2

3

4

5

6

7

ED

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 + 0.12PLAND; 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.



10/12

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 thoseareas, if it follows the general patterns presented by croplands

in this study.

Ecosystem services are processes and conditions by which eco-

systems provide benefits for humans (Costanza et al., 1997). These

services include climate regulation, water and food supply, control

of drought and flood, 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 maintainoriginal 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 affectproduction (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 abiased distribution of remnant fragments in relation to slope. Gen-


dominant cover

0.0

0.51.0

1.5

2.0

2.5

3.0

3.5

Num

bero

ffragmen

ts


dominant cover

0.0

0.51.0

1.5

2.0

2.5

3.0

3.5

Num

bero

ffragmen

ts


dominant cover

0.0

0.5

1.0

1.5

2.0

2.5

3.0

3.5

Num

ber

offragmen

ts


dominant cover

0.0

0.5

1.0

1.5

2.0

2.5

3.0

3.5

Num

ber

offragmen

ts


dominant cover

0.0

0.5

1.0

1.5

2.0

2.5

3.0

3.5

Numbero

ffragments


dominant cover

0.0

0.5

1.0

1.5

2.0

2.5

3.0

3.5

Numbero

ffragments

a

c

e f

d

b

Fig. 8. Numberof fragmentswith area greater than 10 times thehome range of mammalspecies 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 maximusand (f) maned-wolf, Chrysocyon brachyurus.



11/12

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 ResearchCouncil (MCT CNPq) through Grants given to PDM and LGF.

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Carvalho Et Al. 2009 the Cerrado Into-pieces