Biological Conservation 274 (2022) 109737

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

How 30 years of land-use changes have affected habitat suitability and

connectivity for Atlantic Forest species
Milena Fiuza Diniz a, b, *, Marco Túlio Pacheco Coelho c, Ana María Sánchez-Cuervo b,
Rafael Loyola a, d
a
Departamento de Ecologia, Universidade Federal de Goiás, Goiânia, Goiás 74690-900, Brazil
b
Center for Conservation & Sustainability, Smithsonian Conservation Biology Institute, P.O. Box 37012, MRC 705, Washington, DC 20013-7012, USA
c
Swiss Federal Institute for Forest, Snow and Landscape, Birmensdorf, Switzerland
d
Fundação Brasileira para o Desenvolvimento Sustentável, Rio de Janeiro, Rio de Janeiro 22160-180, Brazil

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

Keywords: Land-use changes have severely degraded natural landscapes around the world, constituting the primary driver
Habitat network of biodiversity loss. In recent decades, agriculture expansion and the lack of effective conservation policies have
Forest loss mainly eroded tropical forests. Here, we built multi-scale habitat suitability models to investigate how land-use
Fragmentation
changes in the Brazilian Atlantic Forest over the last 30 years (1989–2019) have impacted habitat suitability and
Multi-scale modeling
Protected area
connectivity for six globally threatened or near-threatened species. We also assessed how the cover of highly
Threatened species suitable forests by protected areas has changed over the study period. We found an average reduction of 10% of
suitable forests for the target species. Our models estimated a loss of up to 37% of highly suitable forests, with
more range-restricted species experiencing the greatest declines. Today, forests still cover most highly suitable
areas found in 1989, however they show reduced suitability due to landscape degradation. Pasture, agriculture,
and forest plantations were the main land uses that replaced highly suitable forests. The land-use changes also
deteriorated the connectivity network for most species. Although the total area protected more than doubled in
the Atlantic Forest, we showed that the highly suitable forests under some level of protection covers only
0.6–2.5% of species extent of occurrence. Our study demonstrates how unplanned land-use changes can erode
forest quantity, quality, and connectivity for threatened species, challenging their long-term persistence. Our
findings reveal the need to expand and improve the protected area network of the Atlantic Forest and highlight
the critical role of land-use planning for protecting biodiversity.

1. Introduction One of the immediate consequences of human activity expansion is

Humanity's demands for space and natural resources have pro­
foundly altered the planet surface and its ecosystems (Foley et al., 2005;
Song et al., 2018). Land-use activities are estimated to be directly
responsible for 60% of all land modifications in recent decades (Song
et al., 2018). These changes have markedly reduced biodiversity
worldwide, with declines in local species richness estimated at up to
76.5% (Newbold et al., 2015). Recent global projections showed that
land-use changes alone might cause substantial shrinkage of the suitable
habitats for terrestrial vertebrates by 2070, resulting in the deteriorating
threat status of approximately 1700 species (Powers and Jetz, 2019).
deforestation. Since 1990, deforestation has caused a global forest loss of
420 million ha. Although the rate of forest loss has declined substantially
in the past decades, about 10 million ha of forest is still lost annually
(FAO, 2020). Among land-use activities, agriculture expansion is
responsible for the largest single cause of native vegetation loss and
global biodiversity decline (Gibbs et al., 2010). During the 1980s and
1990s, more than 80% of expanding agricultural land in the tropics
replaced forests instead of previously cleared areas, 55% of which were
intact forests (Gibbs et al., 2010). Potential biodiversity loss due to the
combined effects of future agricultural intensification and expansion is
expected to be more pronounced in the tropics, where many countries

* Corresponding author at: Center for Conservation & Sustainability, Smithsonian Conservation Biology Institute, P.O. Box 37012, MRC 705, Washington, DC
20013-7012, USA.
E-mail addresses: mifiuzadiniz@gmail.com (M.F. Diniz), marcotpcoelho@gmail.com (M.T.P. Coelho), sanchezam@si.edu (A.M. Sánchez-Cuervo), loyola@ufg.br
(R. Loyola).

https://doi.org/10.1016/j.biocon.2022.109737
Received 20 August 2021; Received in revised form 21 July 2022; Accepted 11 September 2022
Available online 21 September 2022
0006-3207/© 2022 Elsevier Ltd. All rights reserved.
M.F. Diniz et al.
show both high agricultural growth and low conservation spending
(Kehoe et al., 2017).
The deterioration of tropical forests contributes disproportionately
to the impoverishment of global biodiversity because these forests pro­
vide habitat for over half of global biodiversity. However, they occupy
less than 10% of the Earth's land surface (Bradshaw et al., 2009). Even
disregarding other human pressures and species extinction elsewhere,
the estimated rate of biodiversity loss due to habitat loss and degrada­
tion in tropical forests could alone cause a mass extinction event over the
next two centuries (Alroy, 2017; Giam, 2017).
One of the most impactful and increasingly widespread forms of
habitat degradation is fragmentation (Haddad et al., 2015). The frag­
mentation level in the tropics shows that forest continuity has been
compromised by deforestation, a pattern that tends to intensify with
future forest loss (Taubert et al., 2018). Breaking the spatial integrity of
habitat can result in a species decline of 20 to 75% (Haddad et al., 2015),
which is particularly harmful for forest-dependent species (Vetter et al.,
2011; Keinath et al., 2017). A global assessment of habitat fragmenta­
tion for the world's terrestrial mammals showed that species experi­
encing a more fragmented habitat face a higher risk of extinction,
especially those with smaller geographic range sizes (Crooks et al.,
2017). Therefore, assessing how land-use activities have altered habitat
quality and availability for more vulnerable species, such as forest-
dependent ones, is valuable for informing conservation strategies. This
type of study can be critical in highly disturbed regions, such as the
Brazilian Atlantic Forest, where native vegetation cover has been
reduced to 28% (of which 26% are forests and 2% correspond to non-
forest native formations; Rezende et al., 2018), and much of the
remaining forest has undergone an intense fragmentation process
(Ribeiro et al., 2009).
Here we evaluated how the land-use/cover changes in the Brazilian
Atlantic Forest in the last 30 years (2019–1989) have impacted habitat
suitability and connectivity for six globally threatened or near-
threatened forest species. We also identified the main landuses respon­
sible for the loss of highly suitable forests and whether the expansion of
protected areas in the Atlantic Forest could cover essential areas for the
target species. The habitat and connectivity analyses carried out in our
study were based on habitat suitability models built from the application
of a random forest algorithm within a multi-scale approach of how
species respond to different environmental factors (e.g., Zeller et al.,
2018; Ashrafzadeh et al., 2020; Rather et al., 2020a).
2. Materials and methods
We applied a multi-step approach based on building multi-scale
habitat suitability models for the years 1989 and 2019 for each target
species. The summary of the performed analyses can be found in Fig. S1.
2.1. Study area
Formed by a complex of 15 ecoregions, the Atlantic Forest was once
the second-largest forest biome in South America (Olson and Dinerstein,
2002). Its tropical and subtropical forests are distributed over three
countries (Brazil, Paraguay, and Argentina), with Brazil having 92% of
the biome's original territory within its borders (FVSA and WWF, 2017).
The high heterogeneity of environmental gradients found throughout
the Atlantic Forest resulted in an impressive and unique diversity of life
forms, with 30% of the >2000 vertebrates found in the biome being
endemic (Mittermeier et al., 2005).
The high level of endemism combined with intense human pressure
make the Atlantic Forest one of the world's conservation priorities
(Mittermeier et al., 2005). In Brazilian lands, human modification has
significantly degraded the Atlantic Forest for more than five centuries,
resulting in the loss of natural vegetation from most of its original ter­
ritory (Ribeiro et al., 2009; FVSA and WWF, 2017; Rezende et al., 2018).
Although recent time-series analyses have shown that in the last three
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Biological Conservation 274 (2022) 109737
decades forest cover in the Atlantic Forest has remained practically
stable (Souza et al., 2020; Rosa et al., 2021), the area occupied by older
forests has decreased and forest isolation increased in more than a third
of the biome's landscapes (Rosa et al., 2021).
Since colonial Brazil, the opening of areas for agriculture has been
the main driver of deforestation in the Atlantic Forest (Young, 2003).
Today, large scale and subsistence agriculture continue to be the leading
direct causes of forest degradation (FVSA and WWF, 2017). Adding to
the pressures of agricultural commodity markets, the Atlantic Forest
biodiversity shares the territory with >148 million people (FVSA and
WWF, 2017). In Brazil, 72% of the total population lives in 15% of the
territory covered initially by the Atlantic Forest. Most of them are in the
two of the largest urban centers in the South American continent - São
Paulo and Rio de Janeiro cities.
We defined the study area according to the overlap between the
species' extent of occurrence (plus a 30 km buffer) and the Brazilian
Atlantic Forest. The biome limits followed the 2019 biome map
(1:250,000) from the Brazilian Institute of Geography and Statistics
(IBGE – acronym in Portuguese), the same boundaries used by the
MapBiomas Collection 5, the land use/cover database we used to obtain
information on the structure of local landscapes.
2.2. Environmental variables
We selected 13 environmental variables related to climate, topog­
raphy, and landscape composition as potential predictors of species
occurrence. These variables were selected based on species ecology and
previous habitat suitability studies (see Text S1). Climatic predictors
(annual mean temperature - bio1, temperature seasonality - bio4, annul
precipitation - bio12, and precipitation seasonality - bio15) were
downloaded from the WorldClim database (available at https://www.
worldclim.org/) at a resolution of 30 s (~1 km). NASA Shuttle Radar
Topographic Mission (available at https://srtm.csi.cgiar.org/) provided
the digital elevation model at 3-arc second resolution (~90 m) used to
extract the elevation data, from which the others topographic variables
(slope and topographic position index - TPI) were calculated using the R
package ‘raster’ (Hijmans, 2021). Variables describing the composition
of Atlantic Forest landscapes (percentage of forest, non-forest natural
formation, water and wetlands, pasture, agriculture, and urban areas)
were obtained for period of 1989–2019 from the reclassification of the
annual 30-m resolution maps produced by the Brazilian Annual Land
Use and Land Cover Mapping Project (MapBiomas Collection 5; Map­
Biomas, 2020). We aggregated the original MapBiomas classes to obtain
the land use/cover variables according to Table S1. Climatic and land
use/cover variables were adjusted to a spatial resolution of 90 m, the
spatial grain size in which habitat suitability was analyzed and mapped.
To perform a multi-scale analysis, we first summarized all environ­
mental variables in different-sized local landscapes centered in species
occurrence points. After limiting the local landscapes using four
different scales (1, 3, 6, and 12 km), we averaged the values for climatic
and topographic conditions and calculated the proportion of cells in the
buffered area occupied by each land use/cover type. We extracted these
latter variables using the annual layer corresponding to the year in
which species presence was recorded. The candidate scales were chosen
based on the species movement capacity obtained from scientific liter­
ature or estimated using body mass and diet information (Table 1). The
range of tested scales was enough to cover 4 to 9 times the median
distance of dispersal for most species as suggested by Jackson and Fahrig
(2012) and more than enough to delimit a circular area equivalent to
species' home ranges (Table 1). To be able to predict habitat suitability,
we mapped environmental factors throughout the Atlantic Forest
applying a moving window analysis at each scale mentioned above using
the R package ‘raster’ (Hijmans, 2021). For land use/cover variables, we
produced maps considering the different conditions in 1989 and 2019.
M.F. Diniz et al.
Table 1
Extinction risk category of the target species according to Brazilian Red List
(ICMBio/MMA, 2018a) and ecological traits required by the habitat and con­
nectivity analyses. See Text S1 to find the references for species home range and
dispersal. For Alouatta guariba, Mazama nana, and Procnias nudicollis, the
dispersal distances were estimated applying the allometric relationships
described in Sutherland et al. (2000) using the information on body mass and
diet from Wilman et al. (2014). All target species have the same extinction risk
category on the national and IUCN Red List, except Callithrix kuhlii which is
globally listed as Vulnerable and nationally classified as Near Threatened (Neves
et al., 2021).
Species ICMBio Body Dispersalkm Home
masskg rangeha
Alouatta guariba VU 5.2 3.5 33
Bradypus torquatus VU 3.9 1.0 10
Callithrix kuhlii NT 0.3 1.5 34
Leontopithecus EN 0.6 2.0 83
chrysomelas
Mazama nana VU 16.5 6.5 30
Procnias nudicollis NT 0.2 2.0 60a
a
The smallest forest fragment size where the species was registered among the
studies we found from a non-exhaustive literature review.
2.3. Target species
This study focused on endangered and forest-dependent species
inhabiting the Brazilian Atlantic Forest, for which there were adequate
presence data for modeling habitat suitability. To find these species, we
identified endemic birds and mammals to the Atlantic Forest or with
most of their distribution restricted to the biome and classified as
Threatened or Near Threatened according to the latest national extinc­
tion risk assessment (Ministério do Meio Ambiente Decree No. 445 of
2014). From this initial list, we defined as target species those forest-
dependent species that have been threatened by habitat loss and frag­
mentation and had about 30 adequate presence points to model habitat
suitability. We used this cut-off because it is known that the performance
of habitat suitability models decreases severely for sample sizes smaller
than 30 presence observations (Guisan et al., 2017). The application of
all criteria described above resulted in a list of one bird and five mam­
mals (Table 1; Fig. S2). We provided information on target species'
ecology and conservation in Text S1 - Supplementary Material.
2.4. Occurrence data
We searched for species presence data from 1989 to 2019 in the
scientific literature (Lima et al., 2017; Hasui et al., 2018; Culot et al.,
2019; Santos et al., 2019; Souza et al., 2019; Esquivel et al., 2019; Nagy-
Reis et al., 2020), in the Global Biodiversity Information Facility (GBIF,
2021), and the Portal da Biodiversidade (https://portaldabiodiversida
de.icmbio.gov.br/portal/). We did not include presences of fossil spec­
imens from an unknown source or preserved specimens in GBIF. To
ensure the exclusion of coordinates from museums, zoos, and other in­
stitutions that may have individuals in captivity, we excluded all records
present in pixels classified as urban areas according to the land use/
cover map for 2019 provided by MapBiomas (2020). In addition, we
cleaned the records to retain only presences with a maximum spatial
error of 500 m and with information about the sampling year to adjust
the extraction of land use/cover variables to the equivalent MapBiomas
annual map. To reduce spatial clumping of records and correct sampling
bias, we applied a rarefaction procedure excluding all overlapping
presences considering a buffer with a radius of 5 km around them
(Kramer-Schadt et al., 2013).
We created artificial absences (or pseudo-absence) because we could
not find accurate information for the target species. Using R package
‘dismo’ (Hijmans et al., 2020) and following the recommendations made
by Barbet-Massin et al. (2012), we randomly generated pseudo-absences
and retained them in the same amount as the presences. As all target
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Biological Conservation 274 (2022) 109737
species had <100 cleaned presence points, we produced 10 replicate sets
of pseudo-absences (Barbet-Massin et al., 2012). Therefore, we run 10
habitat suitability models for each species resulting from the different
occurrence data (presences + 10 replicates of pseudo-absences). Pseudo-
absences that are taken very distant from the set of presences points are
not very informative (VanDerWal et al., 2009; Barbet-Massin et al.,
2012). Therefore, we sampled pseudo-absences considering the entire
Atlantic Forest for the two widespread species (Alouatta guariba and
Procnias nudicollis). In contrast, for the other species (narrow-ranged
ones), we limited the possible locations of the pseudo-absences to a 500
km buffered area around their geographical range in an attempt to
incorporate uncertainties about the species range and peripheral con­
ditions associated with their absences. Finally, we maintained only
pseudo-absences that were distant 5 km from each other or from any
presence point.
2.5. Habitat suitability modeling
We modeled multi-scale habitat suitability for each species using
random forest (RF), a machine-learning technique based on the boot­
strap aggregation (also known as bagging) of classification and regres­
sion trees (Breiman, 1996, 2001). RF is one of the most used and
recommended algorithms to model species niche and distribution
(Evans et al., 2011; Guisan et al., 2017; Fletcher and Fortin, 2018).
Recently, this technique has gained popularity as a tool to analyze the
habitat relationships of species at multiple scales because of its flexi­
bility compared to parametric and/or traditional statistical approaches
(Cushman and Wasserman, 2018; Fletcher and Fortin, 2018; Ashrafza­
deh et al., 2020; Rather et al., 2020a, 2020b). These multi-scale models
can also be used to create predictive maps of species occurrence from
which it is possible to derive the resistance surfaces used in modeling
wildlife corridors (e.g., Zeller et al., 2018; Ashrafzadeh et al., 2020).
To build multi-scale habitat suitability models, we identified and
adjusted each environmental predictor to the spatial scale at which
species occurrence was best predicted by each environmental compo­
nent (i.e., scale of effect; Jackson and Fahrig, 2012; McGarigal et al.,
2016). For this, we run univariate RF models considering the environ­
mental conditions within local landscapes created from multiple buffers
(with radii of 1, 3, 6, and 12 km) surrounding the occurrence points (e.
g., Ashrafzadeh et al., 2020; Rather et al., 2020b). We ran the univariate
RF models considering the 10 different sets of pseudo-absences for each
species and used the mean out-of-bag (OOB) error rate to describe each
scale's performance. We selected as the scale of effect the one with the
lowest OOB error rate for a given environmental variable.
After modifying each predictor according to their respective scale of
effect, we evaluated the pairwise correlation between scaled variables
(e.g., if for a given target species the scales of effect for mean temper­
ature and % of forest were 12 km and 1 km, respectively, the correlation
between these environmental predictors was tested considering the
spatial layers adjusted to 12 km for temperature and 1 km for forest). For
correlated pairs (|r| > 0.6), we excluded the scaled variable with the
worst fit based on the OOB error rate. From the set of scale-optimized
and nonredundant predictors, we applied the RF model selection
available in the R package ‘rfUtilities’ (Evans and Murphy, 2019) that
implements the procedure proposed by Murphy et al. (2010). In this
approach, model improvement ratio is applied to select the set of vari­
ables that resulted in a model with the best error component based on
the smallest OOB error, lowest maximum within-class error, and fewest
parameters (Murphy et al., 2010). We also performed the model selec­
tion for each model built from the 10 replicates of occurrence data.
Univariate and multivariate RF models were performed using the R
package ‘randomForest’ (Liaw and Wiener, 2002). The number of
randomly sampled predictors at each split (mrty parameter) was opti­
mized for each model using the tuneRF() function. The number of
bootstrapped trees to grow was chosen according to error convergence.
To evaluate the model fit, we computed the OOB error rate, the area
M.F. Diniz et al.
under the ROC curve (AUC), and True Skill Statistic (TSS); the last two
performance measures were obtained from back-predictions. Although
the OOB error rate provides a form of independent validation because
error distribution is assessed from data not used to build RF models,
Evans et al. (2011) recommended the addition of cross-validation
techniques to evaluate model performance against independent data.
Thus, we also evaluated model performance through one-thousand 10-
fold cross-validations using the R package ‘rfUtilities’.
We selected the five models with the lowest OOB error among the 10
models built from the replications of pseudo-absences to predict the
probability of species occurrence for 1989 and 2019. Finally, we pro­
duced an ensemble map for each year using the average suitability
values per pixel for the five predictive maps. We restricted the habitat
suitability maps to a 30 km buffer area around the species extent of
occurrence (EOO; Fig. S2). EOO information was obtained from the
Brazilian environmental agency (Instituto Chico Mendes de Con­
servação da Biodiversidade, ICMBio) for the nationally threatened spe­
cies and from IUCN for the near-threatened species (ICMBio/MMA,
2018b,c; IUCN, 2021).
2.6. Changes in the amount and protection of suitable forests
We evaluated the changes in suitable habitat in the past 30 years
using different habitat suitability thresholds. For this, we calculated the
percentage of loss or gain of suitable forests identified in 2019 in relation
to those present in 1989. We considered as suitable forest those forest
remnants with area equal to or greater than species home range
(Table 1) located within the suitable regions. Fixing the threshold of
probability for species occurrence in 0.9 to find highly suitable forests,
we evaluated the replacement of these areas by land uses during the
analyzed time interval.
We evaluated the differential efficiency of the set of protected areas
established in the two years (1989 and 2019) by computing the per­
centage of highly suitable forests under some level of protection and
comparing it with the general change that occurred throughout the
Brazilian Atlantic Forest. The spatial data and year of creation of the
protected areas were downloaded from the Brazilian Ministry of Envi­
ronment spatial database (http://mapas.mma.gov.br/i3geo/datadow
nload.htm).
2.7. Changes in network connectivity
To quantify how land-use changes affected the connectivity of highly
suitable areas, we first assembled habitat networks individually for the
species. We set as network nodes the highly suitable forest patches with
areas equal to or greater than species' home range and connected them
via least-cost paths (network links), forming a minimum planar graph
network (Fall et al., 2007; Rayfield et al., 2016). To find the least-cost
paths, we converted the habitat suitability maps into resistance sur­
faces using a negative linear function (Zeller et al., 2018).
Finally, we computed the relative change in functional connectivity
using the equivalent connected area index (ECA; Saura et al., 2011),
considering the habitat networks for 1989 and 2019 (Fig. S1). ECA is a
habitat availability index defined as the amount of habitat in a single
patch (maximally connected) that would provide the same connectivity
value as the observed habitat arrangement in the landscape (Saura et al.,
2011). This network-based index incorporates the habitat patch attri­
butes and the spatial arrangement, as well as the target species' dispersal
capacity to provide a functional connectivity measure (Saura and
Pascual-Hortal, 2007; Saura et al., 2011). One of the greatest advantages
of the ECA index is that after a given spatial change in the landscape, the
relative variation in this index (dECA) can be directly compared with the
variation in the total habitat area (dA) to verify how the addition (via
regeneration or restoration) or loss of habitat impacted the network
connectivity (Saura et al., 2011). When the changes in the landscape
produce a dECA < dA, the gain or loss of habitat had a modest
4
Biological Conservation 274 (2022) 109737
contribution to an increase or decrease in network connectivity. The
contrary pattern (dECA > dA) reveals that habitat modification has a
significant impact on connectivity, and a dECA = dA indicates that the
gain or loss of habitat did not affect the network connectivity, i.e. there
was “a neutral area gain in terms of its benefit for connectivity” (Saura
et al., 2011). Here, we computed dECA and dA as the relative variation
between the index values for the habitat networks in 2019 and 1989
compared to the 1989 network.
3. Results
3.1. Scales of effect and habitat suitability models
We found significant heterogeneity at the spatial scales in which
species occurrence responded more strongly to the environmental con­
ditions (Fig. S3). Still, the optimized scales for some predictors were
consistent for most species. For example, the percentage of non-forest
natural formation and precipitation seasonality best explained species
occurrence at 1-km and 3-km scales. In contrast, slope, percentage of
forest, and croplands showed a stronger relationship at broader scales (6
km and 12 km). The scales of effect for mean temperature, mean pre­
cipitation, elevation, and TPI varied widely between species.
The multi-scale random forest models had good to excellent fits
(AUC: 0.82–0.95 and TSS: 0.64–0.9; Table 2). The OOB error rate varied
from 5% to 18% and, like the other performance metrics, presented a
slight variation along the five best models adjusted from different rep­
licates of pseudo-absences (Table 2). One-thousand 10-fold cross-
validations also provided similar error rates (2%–19%), with an
equally balanced error between the classes of presence and absence for
Alouatta guariba, Bradypus torquatus, and Procnias nudicollis (Table S2).
For the other species, the classification error was two to four times lower
for presences than for absences.
All target species were affected by at least one land-use/cover vari­
able (Fig. S4). The percentage of forest covering the pixel neighborhood
(i.e., local landscape) was retained in all models (derived from the five
occurrence replicas) for Alouatta guariba, Bradypus torquatus, Leontopi­
thecus chrysomelas, and Procnias nudicollis, showing high importance for
predicting their occurrences. For Callithrix kuhlii and Mazama nana, the
percentage of forest was selected in three of the five best-fit model
replicas. Leontopithecus chrysomelas and Procnias nudicollis were the
species whose presence was associated with the highest percentage of
forest cover (above 80%).
Temperature seasonality was among the four main predictors for all
species. Species whose occurrences were predicted to be affected by
land-use activities showed negative relationships with increased human
pressures in local landscapes. The percentage of agriculture within a
6–12 km radius was found to have a major negative impact on the
presence of Alouatta guariba, Bradypus torquatus, Callithrix kuhlii, and
Procnias nudicollis, being only tolerated at low occupancy rates (10%–
20%).
Table 2
Average performance metrics (AUC: aera under the ROC curve, TSS: True Skill
Statistic, OOB: out-of-bag error rate) using back-prediction to the data for the
five models with the lowest OOB error adjusted from the filtered presence re­
cords (N) and different replicates of pseudo-absences. The standard deviation is
shown in parentheses.
Species N AUC TSS OOB
Alouatta guariba 83 0.82 (0.01) 0.64 (0.02) 0.18 (0.01)
Bradypus torquatus 53 0.95 (0.01) 0.89 (0.02) 0.05 (0.01)
Callithrix kuhlii 50 0.87 (0.01) 0.74 (0.03) 0.13 (0.01)
Leontopithecus chrysomelas 34 0.89 (0.01) 0.78 (0.02) 0.11 (0.01)
Mazama nana 28 0.95 (0.02) 0.90 (0.04) 0.05 (0.02)
Procnias nudicollis 52 0.88 (0.02) 0.76 (0.03) 0.12 (0.02)
M.F. Diniz et al.
3.2. Changes in suitable habitat
Considering suitable forests as those with >0.7 probability of pres­
ence inside fragments capable of harboring at least a species home
range, there was an average forest loss of 10.3% (sd = 6.26, range =
1.4%–19.5%) between 1989 and 2019 for the target species (Fig. 1).
Patterns of change in the quantity of suitable forests between 1989 and
2019 were consistent whether or not the home range size was applied as
a size filter for selection of forest fragments (Figs. 1, S5), variating from
+12.3% to -36.6% among the species and thresholds (Fig. 1). In general,
all species showed a decrease in the suitable forest regardless of the
chosen threshold, except Alouatta guariba, for which there were gains of
2.7% and 12.1% in suitable forest considering the two highest thresh­
olds (0.8 and 0.9), respectively. The species with the most restricted
distribution, Callithrix kuhlii and Leontopithecus chrysomelas, showed the
most significant decline in highly suitable forests (0.9 threshold) in the
last 30 years, showing reductions of 36.6% and 20.1%, respectively.
Most of the area that suffered loss of highly suitable forest between
1989 and 2019 remains covered by forests, but whose conditions of the
surrounding landscape have been degraded (Fig. 2). Bradypus torquatus,
Mazama nana, and Leontopithecus chrysomelas presented the highest
percentage of suitable forests directly replaced by land-use activities,
mainly pasture and agriculture. About 10% of the highly suitable forests
for Mazama nana and Procnias nudicollis were occupied by forest plan­
tations. This land-use activity also led to a decline of 7% in the highly
suitable forest for Alouatta guariba.
3.3. Trends in the landscape connectivity
The relative variation in the equivalent connected area index (dECA)
and the total area of highly suitable forest (dA) showed that the spatial
modification caused by land-use changes in 1989–2019 resulted in the
deterioration of network connectivity for Bradypus torquatus, Mazama
nana, Leontopithecus chrysomelas, and Procnias nudicollis (Fig. 3). The
decline in forest connectivity was substantially more pronounced for the
Fig. 1. Changes in suitable forest area in 2019 compared to 1989 according to different probability thresholds. We considered only forest fragments with an area
equal to or greater than the size of the species home range. Habitat suitability was mapped at a spatial resolution of 90 m.
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Biological Conservation 274 (2022) 109737
first three species, with decreases 47.5%–26.9% greater compared to
forest area loss. The opposite trend occurred for the Alouatta guariba
network, where increases in highly suitable forests also resulted in an
improvement of connectivity. For Callithrix kuhlii, the severe habitat loss
caused by changes in land-use activities over the past 30 years was
accompanied by a nearly equivalent decline in connectivity.
3.4. Protected area cover
The percentage of the original territory of the Brazilian Atlantic
Forest within protected areas more than doubled in the last 30 years,
increasing from almost 4% to about 9% (Fig. 4). To a greater or lesser
extent, all target species have benefited from this expansion since there
was a large increase in the percentage of highly suitable forests under
some degree of protection. Despite this, the highly suitable forests that
are currently protected represent about 0.6–2.5% of the target species
EOO.
4. Discussion
4.1. Multi-scale conservation assessment and planning
In agreement with other multi-scale habitat modeling studies (e.g.,
Ashrafzadeh et al., 2020; Rather et al., 2020a), our results showed that
habitat selection predictions are scale sensitive, with different envi­
ronmental factors affecting species at different spatial scales. While
some predictors showed stronger relationships at larger scales (6 km and
12 km, e.g., slope, percentage of forest, and croplands), other predictors
showed stronger relationships at finer ones (1 km and 3 km, e.g., per­
centage of non-forest natural formation and precipitation seasonality).
Whereas the great majority of studies in wildlife conservation do not use
a multi-scale approach (McGarigal et al., 2016), our study reinforces
that inferences for conservation planning and management must adopt
multi-scale predictors for better accuracy and precision on conservation
actions and for avoiding inefficient or ineffective strategies (Poor et al.,
M.F. Diniz et al.
Fig. 2. Land use/cover types occupying areas that were estimated to be covered by highly suitable forests for each target species in 1989 that were no longer
classified as such in 2019.
Fig. 3. Percentage of decrease or increase in the total area (dA) and connec­
tivity of the network formed by highly suitable forests (measured via dECA) for
each target species in 2019 relative to 1989 caused by land-use modifications.
2020). For example, the percentage of agriculture within a 6 to 12 km
radius negatively impacted four species occurrences and was tolerated
at low occupancy rates (10–20%). Mitigating the adverse effects of this
human pressure requires an appropriate spatial dimension of conser­
vation actions on land use planning. Therefore, habitat suitability
models aiming to guide conservation actions should include landscape
descriptors, such as those of land cover and land use used in this study,
preferably considering the scales of effect (e.g., Diniz et al., 2022). The
non-inclusion of these variables may overestimate the amount of suit­
able habitat, mainly for medium and high forest dependent species, as
observed for Atlantic Forest birds (Oliveira-Silva et al., 2022).
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Biological Conservation 274 (2022) 109737
Fig. 4. Percentage of the species' extent of occurrence (EOO) covered by highly
suitable forests under some degree of protection in 1989 and 2019.
4.2. Losing quantity and quality of suitable forests
For the past 30 years, our analysis estimated an average loss of 10%
of suitable forest area (identified using a threshold of 0.7 for predicting
species occurrence) and up to about 37% reduction of the highly suitable
forest area (identified using a threshold of 0.9). The two species having
the most restricted distribution, Callithrix kuhlii and Leontopithecus
chrysomelas, showed the greatest declines. These species of small pri­
mates have great overlap in their geographic ranges, both located in the
south of Bahia, one of the Brazilian states that has stood out due to the
large area of Atlantic Forest lost annually in the last decades (SOS Mata
Atlântica and INPE, 2022).
M.F. Diniz et al.
In the context of our study, the observed decrease in suitable forests
was caused by two processes, the direct loss of the forest area or the
reduction of forest suitability via local landscape degradation. Both
processes were driven by expanding land-use activities, mainly pasture,
agriculture, and forest plantation in the last three decades. These results
are consistent with current land occupation (2017) in areas of native
forest loss in the Brazilian Atlantic Forest, where 81% of the deforested
area is recently occupied by agriculture and pasture and 16% by
monoculture tree plantations (Rosa et al., 2021). Without effective
conservation efforts, the loss of forest quantity and quality is likely to
continue as the role of agriculture as a major driver of biodiversity
decline is expected to be reinforced by the increasing global need for
crop production (Tilman et al., 2011).
The rapid conversion of native vegetation to agriculture and other
non-forest land uses represents the main threat to Brazilian birds and
mammals according to the latest national extinction risk assessment
(ICMBio/MMA, 2018b,c). Especially in the case of the Atlantic Forest
that has already lost most of its forest cover and is the Brazilian biome
with the highest number of threatened animal species (593 species, of
which 76% are endemic; ICMBio/MMA, 2018a), our observations
reinforce that the continuous loss of suitable forests can rapidly deteri­
orate the conservation status of many species. In addition to habitat loss
and degradation, the persistence of threatened species in the Atlantic
Forest is still challenged by hunting, animal trade, infectious diseases,
roadkill, invasive species, and climate change (ICMBio/MMA, 2018a;
Galetti et al., 2021). Severe reductions of the target species population
mean losing essential ecosystem functions and services such as seed
dispersal (Pizo et al., 2002; Bufalo et al., 2016; Chaves et al., 2018).
Local or functional extinction of large-bodied dispersers, such as pri­
mates (e.g., Leontopithecus chrysomelas and Alouatta guariba) and cotin­
gas (e.g., Procnias nudicollis), has a strong negative impact on forest
regeneration (Gardner et al., 2019), carbon storage (Bello et al., 2015),
and even on evolutionary trajectories of key life-history traits of tropical
plants (Galetti et al., 2013).
A. guariba was the only species for which there was an increase in
highly suitable forests (12%) in the last decades. This result can be
explained by the joint effect of land use/cover variables on the species
occurrence, its geographic distribution, and the spatial patterns of land
use/cover changes in the Atlantic Forest in recent decades. According to
our habitat model, the presence of this species is mainly associated with
large forest cover (above 50%) and low occupation of croplands (below
20%) in 12-km local landscapes (Fig. S4-a). Although the cropland area
has doubled in the Brazilian Atlantic Forest in the past 30 years, this
expansion occurred mainly over pasturelands (Souza et al., 2020; Rosa
et al., 2021). Many landscapes (most of them within the distribution of
A. guariba located in southeastern Brazil) showed gains in forest cover
and reduction in isolation between 1990 and 2017 (Rosa et al., 2021),
which may also explain the increased connectivity for the species esti­
mated by our analysis. Nevertheless, the apparent stability of the
Atlantic Forest cover (varying between 28 and 30 Mha in 1989–2018) in
recent decades (with forest cover gain in some landscapes) has masked
the rejuvenation of the forest cover, as the continuous loss of older
forests has been offset by the gain of younger forests, a process with
negative consequences for the conservation of biodiversity (Rosa et al.,
2021). Even though A. guariba is tolerant to environmental changes and
anthropogenic disturbances, therefore not being restricted to the pri­
mary forest (Jerusalinsky et al., 2021), the long-term persistence of
small and isolated populations under such conditions is not guaranteed,
which could compromise the regional persistence of the species (Bicca-
Marques et al., 2020).
Furthermore, as A. guariba has a wide distribution, the observed
gains in area and connectivity of highly suitable forests disproportion­
ately benefit its southern subspecies (A. guariba clamitans), while a
contrary pattern of forest loss and isolation must be observed for the
northern subspecies (A. guariba guariba, listed globally and nationally as
Critically Endangered). This because A. guariba guariba has a much more
7
Biological Conservation 274 (2022) 109737
restricted distribution, with a large portion overlapping the south of
Bahia, an area that has been intensely deforested and fragmented in
recent decades, as previously mentioned. Habitat loss and fragmentation
caused mainly by the expansion of eucalyptus and coffee monocultures
are among the main threats faced by small subpopulations of A. guariba
guariba (ICMBio/MMA, 2018b).
4.3. Land-use changes have made forests more isolated
In addition to reducing suitable areas, we found that the network of
highly suitable forests became more disconnected for most target species
due to land-use changes in the last 30 years. This decrease in connec­
tivity occurred mainly for Bradypus torquatus, Mazama nana, and Leon­
topithecus chrysomelas, with reductions up to 47% greater compared to
forest loss. Increased forest isolation can have particularly negative
impacts on B. torquatus populations due to the species' low metabolism
(which directly affects its ability to disperse) and low tolerance to high
altitude locations (preferring from sea level to 300 m), a condition
typically found in the mountainous regions within their EOO (Hirsch
and Chiarello, 2012).
A decrease in connectivity over time is a standard expectation in
highly fragmented landscapes because of the poorly planned nature of
land-use change (Dobson, 1997; Diniz et al., 2021; Etter et al., 2006).
However, the consequences for biodiversity can be drastic if this sce­
nario is not reverted over the next decades (Haddad et al., 2015). The
movements of individuals across populations avoid isolation and
decrease the risk of inbreeding depressions (Kremen and Merenlender,
2018). Connectivity is essential for maintaining viable populations over
time, but it is also crucial to mitigate climate change (Heller and
Zavaleta, 2009). With ongoing climate change, species are moving to
follow their optimum climatic conditions (Pecl et al., 2017). Still, if they
are not capable to cross human-modified habitats, climatic selection
pressure might lead to local extinctions, especially in isolated areas
(Heller and Zavaleta, 2009). Terrestrial mammals have shorter dis­
placements in human-modified habitats (Tucker et al., 2018), which
makes the improvements of connectivity for the species analyzed here
critical and challenging for conservation.
4.4. Protection has increased but is still insufficient
Although the original territory of the Brazilian Atlantic Forest within
protected areas more than doubled over the last decades, we found that
the current amount of the highly suitable forest areas under some level
of protection represents <3% of the species EOO. This shows that
despite the recent effort to increase the protection of essential ecosys­
tems in the Atlantic Forest (an additional area of 2,136,221 ha between
2000 and 2015, representing a 27% increase; FVSA and WWF, 2017;
Rezende et al., 2018), the highly suitable forests for the target species
are underrepresented by the current system of protected areas. Because
protected areas are pillars to decrease biodiversity loss (Watson et al.,
2014), the small representation of suitable forests shows the need to
expand and improve the Atlantic Forest system. In addition, it is critical
that ecological corridors are conserved and restored between protected
suitable forests, thus increasing the habitat availability for species. For
this, connectivity planning in areas of great socioeconomic interest, as in
many parts of the Atlantic Forest, must consider both multispecies re­
quirements and human demands, as was done for the protected areas of
the Paraguayan Atlantic Forest (Diniz et al., 2022). For this, our study
reinforces the need to consider land-use planning and different man­
agement strategies in the appropriate spatial dimension, as well as
future environmental changes so that conservation actions can provide
habitat and connectivity for the long-term persistence of species.
CRediT authorship contribution statement
Milena Fiuza Diniz: Conceptualization, Investigation,
M.F. Diniz et al.
Methodology, Formal analysis, Visualization, Writing – original draft,
Writing – review & editing. Marco Túlio Pacheco Coelho: Conceptu­
alization, Writing – original draft, Writing – review & editing. Ana
María Sánchez-Cuervo: Conceptualization, Supervision, Writing – re­
view & editing. Rafael Loyola: Conceptualization, Supervision, Writing
– review & editing.
Declaration of competing interest
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influence
the work reported in this paper.
Data availability
Data will be made available on request.
Acknowledgments
MFD and RL research was funded by CNPq (grant #150488/2019-
0 and grant #306694/2018-2, respectively). This paper is a contribution
of the INCT in Ecology, Evolution and Biodiversity Conservation funded
by MCTIC/CNPq (grant #465610/2014-5) and FAPEG (grant
#201810267000023). MTPC acknowledges funding support from the
Swiss National Foundation (SNF, No 197753) granted to C. H. Graham.
Appendix A. Supplementary data
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.biocon.2022.109737.
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