Forest Ecology and Management 481 (2021) 118704

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Forest Ecology and Management

journal homepage: www.elsevier.com/locate/foreco

Landscape composition is more important than local vegetation structure

for understory birds in cocoa agroforestry systems
Júlia Perez Cabral *, Deborah Faria , José Carlos Morante-Filho *
Applied Conservation Ecology Lab, Programa de Pós-graduação em Ecologia e Conservação da Biodiversidade, Universidade Estadual de Santa Cruz, Rodovia Ilhéus-
Itabuna, km 16, Salobrinho, 45662-000 Ilhéus, Bahia, Brazil

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

Keywords: Biodiversity-friendly agricultural systems allow the maintenance of native species even in highly fragmented
Agrosystems landscapes by providing corridors to species dispersion and offering supplementary resources for animal pop­
Anthropogenic landscapes ulations. In the tropical region, cocoa agroforestry systems are of great importance for biodiversity conservation
Avifauna
as they maintain part of the native vegetation, and therefore can be used by the local fauna. In this system,
Fragmentation
Habitat loss
understory of native forests is replaced by cocoa trees, which are shaded by large old-growth trees. However, the
Tropical forest persistence of native species in cocoa agroforests depends on local vegetation characteristics but also the land­
scape structure in which these systems are located. Here, we investigated the influence of landscape composition
(i.e. amount of forest cover, cocoa agroforestry and cattle pasture) and local vegetation structure (i.e. number of
native and cocoa trees, basal area of native trees and canopy closure) on understory birds in 18 cocoa agro­
forestry systems located in three regions in the Brazilian Atlantic forest, presenting distinct land use contexts.
Specifically, we assessed the effects of these landscape and local features in predicting richness and abundance
patterns of the entire community, and also in distinct ecological groups, such as forest-dependent and non-forest-
dependent birds, and insectivores, frugivores, and omnivores. Using generalized linear models and Akaike in­
formation criterion, we observed lower species richness of complete community, non-forest and omnivorous
birds in the most deforested region. Also, our findings demonstrated that cocoa agroforests integrated in more
forested landscapes harbor greater richness and abundance of frugivorous birds. Conversely, the increase in
cattle pasture amount at the landscape had a harsh effect on all bird groups evaluated. Regarding local vege­
tation, we observed that the increase of canopy closure leads to greater abundance of insectivorous birds in cocoa
agroforestry systems. Similarly, abundance of non-forest species increased in agroforests with higher number of
cocoa trees. Our study demonstrated that cocoa agroforestry systems can provide complementary habitats for
many species, including forest birds, and therefore can mitigate the effects of habitat loss. However, this key
benefit for bird conservation will be more effective when these agroforestry systems are located in more forested
landscapes, with low amount of cattle pastures. Our findings therefore reinforce the alarming need to maintain
and recover landscape-scale forest amount to ensure species persistence of birds in anthropogenic landscapes,
even in those comprising biodiversity-friendly land uses such as cocoa agroforestry systems.

1. Introduction processes adversely affecting biodiversity, population persistence in

Natural environments are being converted to human-modified
landscapes (Fahrig, 2003; Curtis et al., 2018), especially in the tropics,
were climatic conditions favor agriculture and livestock (Malhi et al.,
2014). Such changes in land use affect the amount and structure of
natural forests that, mainly due to fragmentation and habitat loss, are
becoming smaller and more isolated within human-modified landscapes
(Fahrig, 2003). Although habitat loss and fragmentation are different
such landscapes is frequently a result of their interaction (Fahrig, 2003;
Pardini et al., 2010; Watling et al., 2020). Together, both processes
shape the anthropogenic landscapes composed of forest fragments of
different sizes and disturbance levels, usually inserted in the homoge­
neous matrix dominated by agricultural systems (Malhi et al., 2014;
Morante-Filho et al., 2016). These landscape changes may cause harsh
effects on biodiversity, including population declines and increased risk
of species extinction, mainly due the decrease in the availability and

* Corresponding authors.
E-mail addresses: juliaperezcabral@gmail.com (J.P. Cabral), deborahuesc@gmail.com (D. Faria), jcmfilho9@hotmail.com (J.C. Morante-Filho).

https://doi.org/10.1016/j.foreco.2020.118704
Received 18 June 2020; Received in revised form 31 August 2020; Accepted 13 October 2020
0378-1127/© 2020 Elsevier B.V. All rights reserved.
J.P. Cabral et al.
quality of the remaining habitat (Laurance et al., 1997). Therefore, in
highly deforested landscapes, the matrix features (e.g., the matrix types
and nature of predominant matrix) act as major ecological filters, ulti­
mately determining species dispersal among fragments and serving of
supplementary habitat in periods of scarce resources (Tscharntke et al.,
2012; Malhi et al., 2014).
In tropical forest landscapes, the expansion of cattle pastures and
crop monocultures are the most frequent cause of population decline,
species extinction and alteration of ecological processes (Fahrig, 2003;
Melo et al., 2013; Laurance et al., 2014). Additionally, forest loss and the
increasing isolation of forest patches hamper species biological flows in
anthropogenic matrices, which may lead to additional stochastic losses
(Rosenzweig, 1995). Several studies have documented that habitat
generalist species are more likely to use anthropic matrices to maintain
their fundamental activities, such as foraging and reproduction sites,
than forest specialist species (Waltert et al., 2005; Bonier et al., 2007; da
Silva et al., 2015). Indeed, the high habitat specialization and low
vagility from forest-dwelling species often increase their vulnerability to
disturbances (Clough et al., 2009). Therefore, matrix features can shape
the dynamics of native species populations in fragmented landscapes
(Fischer et al., 2013; Bohada-Murillo et al., 2020). In this context,
agroforestry systems can perform a key role for maintaining biodiversity
in these landscapes (Perfecto et al., 1996). These agrosystems provide a
more structurally complex habitat compared to land uses devoid of
arboreal vegetation (Schroth et al., 2004), conferring a greater land­
scape permeability to most species, including forest-dwellers.
In particular, agroforests are composed of native tree species that
retain part of the local structure of a forest, such as big trees that increase
the shading of the understory layer, and therefore create a more favor­
able microclimate, as well as produce a greater amount of resources for
the fauna (Greenberg et al., 2008). These features allow the mainte­
nance of species diversity (Schroth et al., 2011) and ecological pro­
cesses, including carbon storage (Schroth et al., 2014), being hence
considered more biodiversity-friendly than conventional farming sys­
tems (Perfecto and Vandermeer, 2008; Martin et al., 2020). However,
management intensification of agroforestry through the removal of large
trees may reduce the capacity of these systems to maintain biodiversity,
especially due to the simplification of vegetation structure (Steffan-
Dewenter et al., 2007; Bohada-Murillo et al., 2020). For instance, several
studies documented that local intensification of coffee and cocoa agro­
forestry to increase crop production has drastically reduced native tree
richness and shade levels, putting at risk the animal species that use
these systems (Vandermeer, 2011). Similary, agroforestry systems
located in landscapes with low representation of native remnants are
unable to maintain regional species diversity (Faria et al., 2006, 2007).
Therefore, environmenal factors acting at multiple scales can be pivotal
to understand the capacity of agroforestry to maintain species diversity
in human-modified landscapes.
Although many studies have shown that several bird species can
occur in agroforests (Faria et al., 2006; Van Bael et al., 2008; Cassano
et al., 2009; Clough et al., 2009), the persistence of their populations
depends on the local characteristics and landscape composition in which
these systems are inserted (Harvey and Villalobos, 2007). Also, bird
responses may depend on species’ ecological traits, even among those
groups of species, such as forest-dependent birds, usually considered to
be sensitive to anthropogenic disturbance (Clough et al., 2009). Several
studies highlighted the importance of dietary niche and trophic level as
factors that influence the species sensitivity to disturbance (Bregman
et al., 2014). For instance, specific trophic guilds, such as understory
insectivorous birds (Sekercioglu et al., 2002) and large frugivorous birds
(Sekercioglu et al., 2004), are likely to be the first groups to disappear in
deforested landscapes. However, the proneness of extinction can vary
even among sensitive species. In particular, frugivorous birds show a
greater vagility and ability to use complementary habitats to obtain food
(Moran and Catterall, 2014) compared to insectivorous species, which
require specific local characteristics in forest patches (Stouffer and
2
Forest Ecology and Management 481 (2021) 118704
Bierregaard, 1995).
Here, we evaluated the potential contribution of cocoa agroforestry
systems to maintain understory bird communities in tropical deforested
landscapes. Specifically, we investigated the influence of landscape
composition (i.e. amount of forest cover, cocoa agroforestry and cattle
pasture) and local vegetation structure (i.e. number of native and cocoa
trees, basal area of native trees and canopy closure) on understory birds
in 18 cocoa agroforestry systems located in three regions in the Brazilian
Atlantic forest, presenting distinct land use contexts. We assessed the
effects of landscape and local predictors on bird community richness and
abundance, but also in distinct ecological groups, such as forest-
dependent and non-forest-dependent birds, and insectivores, frugi­
vores, and omnivores. For this, we tested three hypotheses: (i) richness
and abundance of the complete community would be negatively influ­
enced by the simplification of local vegetation and the decrease of forest
cover amount at the landscape scale; (ii) richness and abundance of
forest-dependent birds would be reduced in more intensively managed
cocoa agroforestry (i.e. presenting a lower number of native tree and
hence a greater canopy openness, and a greater density of cocoa trees)
and located in deforested landscapes, while non-forest dependent birds
would show an opposite response; (iii) trophic guilds would respond
differently to changes in local and landscape features. In particular, we
would expect to observe a drastic decrease on both richness and abun­
dance of insectivorous birds in highly managed cocoa agroforestry,
particularly in farms located in deforested landscapes dominated by
cattle pastures (Stouffer and Bierregaard, 1995; Sekercioglu et al., 2002,
2004). Conversely, we would expect to find an increase of richness and
abundance of non-forest birds, mainly omnivorous species, in these
agroforests (García et al., 2007).
2. Methods
2.1. Study area
This study was conducted in southeastern Bahia State, a region
originally dominated by Brazilian Atlantic forest. However, land use
changes over the last 40 years have created human-modified landscapes
mainly composed of a mosaic of secondary forests, cocoa (Theobroma
cacao) agroforestry, rubber tree (Hevea brasiliensis) and eucalyptus
(Eucalyptus sp.) plantations, as well as cattle pastures (Morante-Filho
et al., 2016). The average annual temperature is 24 ◦ C, and annual
rainfall averages 2000 mm/yr. Although there is no significant seasonal
climatic variation, a rainless period may occur from December to March
(Thomas et al., 1998).
Using the ArcGIS software and satellite images (QuickBird and
WorldView from 2011; RapidEye from 2009 to 2010), we created digital
maps with a scale of 1:10 000, which is adequate for identifying land
cover patches based on the visual inspection of differences in color,
texture, shape, location and context. In addition, we also performed an
intensive field validation effort to check and confirm land use classes,
mainly cocoa agroforests, combining current Google Earth imagery.
Then, we randomly selected 18 agroforestry sites, separated by at least 2
km from each other, along a gradient of forest cover amount (from
3.45% to 66.74%), located in three regions presenting different land use
contexts (Fig. 1). The northernmost region is characterized by moderate
forest cover (49%), high cocoa agroforestry cover (28%), and low
extension of open areas (8%) [hereafter, high agroforestry cover (HAC)
region]. The region located in the central portion of our study area
(Fig. 1b) presents high forest cover amount (57%), mainly concentrated
around the Una Biological Reserve and the Una Wildlife Refuge – two
federally protected conservation units that have a total area of 34,804
ha. This region is highly heterogeneous although the matrix is domi­
nated by cocoa agroforestry systems (22%) and rubber trees plantations
(10%) [hereafter, high forest cover (HFC) region]. In contrast, the
southernmost region is highly deforested, presents only 34% of forest
cover, and the matrix is notably more homogeneous, being dominated
J.P. Cabral et al. Forest Ecology and Management 481 (2021) 118704

Fig. 1. Sampling sites (black dots) located in southeastern Bahia State, Brazil. In (A), we show a high agroforestry cover (HAC) region, whose matrix is predomi­
nantly formed by cocoa agroforestry systems. In (B) we show the high forest cover (HFC) region, composed especially by forest remnants. In (C), we highlight the low
forest cover (LFC) region, composed of small forest patches surrounding by cattle pastures, and low amount of cocoa agroforestry systems.

3
J.P. Cabral et al.
by pastures (60%) for extensive livestock production, eucalyptus plan­
tations (5%), and a small amount of cocoa agroforestry (1%) [hereafter,
low forest cover (LFC) region] (Fig. 1c).
2.2. Landscape metrics and scales of effect
Using a patch-landscape approach, we evaluated response variables
within cocoa agroforestry sites, and measured landscape attributes
within a specific radius (buffer) from the center of each focal site
(McGarigal and Cushman, 2002; Fahrig, 2013). We used ArcGIS to es­
timate the percentage of old-growth and secondary forest (forest cover,
hereafter), cocoa agroforestry and cattle pasture around each site; all
metrics related to the landscape composition. We chose these metrics
because previous studies have detected their influence on bird diversty
in human-modified tropical forest landscapes (Reino et al., 2009;
Morante-Filho et al., 2016; Boesing et al., 2018).
Because the effect of landscape variables on biodiversity depends on
the spatial scale at which predictors are measured (i.e. the so-called
“scale of effect”, Fahrig, 2013; Jackson and Fahrig, 2015), we calcu­
lated each landscape metric within 9 different-sized buffers drawn from
the center of each site, ranging from 200 to 1000 m radius (Appendix A
in Supplementary material). We then used linear models to identify
which landscape size was most appropriate to assess the effect of each
landscape predictor on patterns of bird richness and abundance (see
results in Appendix A).
2.3. Local vegetation structure
In the center of each cocoa agroforestry site, we established one 100
× 25 m plot and recorded all old-growth trees with a diameter at breast
height (DBH) ≥ 10 cm, estimated the basal area (m2/ha) and recorded
the number of cocoa trees, regardless of height or DBH. We also esti­
mated the percentage of canopy closure inside each plot using five
hemispherical photographs (Nikon Coolpix 4300 digital camera equip­
ped with hemispherical fisheye lens [Nikon Corp, Tochigi, Japan]),
taken at 1.3 m from the ground and 20 m apart from each other. The
photos were taken between cocoa individuals, as our objective was to
estimate the shading performed only by canopy trees. These photos were
analyzed using Gap Light Analyzer software (Frazer et al., 1999), and
then the mean value of the fives photos were considered as our estimate
of canopy closure (in percentage) in each site. Altogether, these vari­
ables were considered as a proxy of the intensity of local management in
these cocoa agroforests. Specifically, we expected to obtain in highly
managed cocoa agroforests, a smaller number of native trees and thinner
trees, and a greater number of cocoa individuals, which will create a
greater canopy openness.
2.4. Bird surveys
We sampled understory birds in two field seasons (January to July
2019), using the mist-net method (Karr, 1981). Bird sampling was un­
affected by period of survey because our region does not present a
seasonal climatic variation throughout the year (Thomas et al., 1998). In
each agroforestry, we used 10 mist-nets with a total of 120 m long (each
net with 12 m long, 2.5 m high and 31 mm mesh) to capture birds during
three consecutive days per season. The mist-nets were opened from
06:00 a.m. to 04:00p.m., covering the period of activity of the diurnal
birds, and reviewed every 30 min in order to reduce the catch stress. We
avoided sampling on rainy and windy days because such conditions
reduce bird movement and therefore may interfere in the capture suc­
cess. Each captured bird was temporarily marked on one of the right-
wing primary feathers with non-toxic material to avoid recounting the
same individual during sampling. Then, individuals were identified
following the scientific nomenclature of the South American Committee
for classification (Remsen et al., 2014). In this study, we obtained a total
sampling effort of 60 h per agroforestry site.
4
Forest Ecology and Management 481 (2021) 118704
We subsequently classified birds either as forest-dependent or non-
forest-dependent species (hereafter, forest birds and non-forest birds)
based on Stotz et al., 1996 and Bregman et al., 2014 (Appendix B). Forest
birds are considered highly specialized on forest resources, and included
endemic species of the Atlantic forest and those inhabiting forest in­
teriors. Yet, non-forest birds do not depend on forest resources, and
comprised those species reported in a variety of habitat types including
forest edges, open vegetation and anthropogenic areas, such as crop
plantations and pasture. Also, bird species were grouped according to
their trophic guild (i.e., insectivores, frugivores, nectivores, omnivores,
and granivores, see Appendix B). Trophic categories reflect the main
food source of the species, and each bird species was categorized as
omnivores if the diet was composed of different food items. These
classifications were based on our prior knowledge about the ecology and
information available in the literature for each species (Wilman et al.,
2014). For subsequent analyses, we used the information only of the
three most recorded guilds - insectivores, frugivores, and omnivores.
2.5. Statistical analyses
We used generalized linear models to evaluate how richness and
abundance of bird complete communities and different ecological
groups are influenced by environmental predictors. Our models were
composed by only three predictor variables, which included two envi­
ronmental descriptors (one local and one landscape predictor) and study
region as a categorical factor due to contrasting surrounding land-use
contexts observed. We also created non-interactive models due to our
limited sample size. For each response variable, we checked the variance
inflation factor (VIF) to test the multicollinearity between predictors for
each model and then removed those variables presenting VIF ≥ 5 (Zuur
et al., 2009).
We fitted a null model for each response variable to verify if the
models were better than would be expected by chance. We subsequently
used Akaike Information Criterion corrected for small samples (AICc)
and Akaike weight (i.e. the normalized relative likelihood of each
model) to select the best model for each response variable (Anderson,
2008). The model presenting the lowest AIC value was considered the
most plausible one, and all models presenting a lower than two unities
difference in AIC with similar Akaike weight were considered parsi­
monious. In this case, we selected the simplest model, i.e. the model with
fewer parameters. Yet, we always selected the null model when it was
among the most plausible models, because we believe that there is no
simpler model to explain a given pattern than chance.
We also evaluated the fit of the best models using the ratio between
residual deviation and residual degrees of freedom, where values >1
indicate overdispersion, i.e. variation in the data is larger than the mean
(Zuur et al., 2009). We further fitted the models that presented over­
dispersion using the Quasi-poisson family. Furthermore, we evaluated
the spatial autocorrelation in the residuals of the best models based on
the Moran’s I autocorrelation coefficient (Appendix D). All statistical
analyses and graphs were carried out in R software version 3.5.3 (R Core
Team, 2019) using the packages lme4 (Bates et al., 2015), MASS (Ven­
ables and Ripley, 2002), car (Fox and Weisberg, 2019), mgcv (Wood,
2017), nlme (Pinheiro et al., 2020), and AICcmodavg (Mazerolle, 2016).
3. Results
We captured 625 birds in 18 cocoa agroforestry systems, belonging
to 24 families and 64 species. The families Thraupidae (10 species),
Trochilidae (9 species) and Tyrannidae (8 species) showed the highest
species richness and Pipridae (n = 173), Turdidae (n = 113) and Tro­
chilidae (n = 110) presented the highest abundance recorded. The most
abundant species captured was Manacus manacus, with 103 individuals,
followed by Glaucis hirsutus (n = 88), Turdus leucomelas (n = 68) and
Euphonia violacea (n = 47). We captured 365 forest birds belonging to 34
species and 260 non-forest birds belonging to 30 species. Additionally,
J.P. Cabral et al. Forest Ecology and Management 481 (2021) 118704

insectivorous birds comprised the trophic guild most recorded (22 spe­ Table 1
cies, n = 86), followed by omnivores (15 species, n = 174), and frugi­ Best models (ΔAICc ≤ 2) used to explain the relationship between richness and
vores (13 species, n = 243). abundance of bird ecological groups and several environmental predictors
Our results highlighted several parsimonious models (ΔAICc ≤ 2) for recorded in 18 cocoa agroforestry systems located in the Brazilian Atlantic
explaining the effects of environmental predictors on understory bird forest. When several parsimonious models were indicated, we selected the
simplest model (i.e. the model with fewer parameter - k). The significative
communities (Table 1; Appendix C). Additionally, we did not detect
predictors (P ≤ 0.05) in each model are highlighted in bold (more details in
spatial autocorrelation in the residual of all best models (Appendix D),
Appendix C).
indicating independence among sampling sites. We observed a harsh
Bird groups Response Models k Wi
effect of study region on the diversity of some bird groups, especially in ΔAICc
variables
species most adapted to disturbances (Appendix E). Specifically, we
observed lower species richness of complete community, non-forest and Complete bird Richness Abundance of cocoa 0.00 3 0.21
community trees + Cattle pasture
omnivorous birds in the more deforested region (LFC region). This re­
Cattle pasture 0.71 2 0.15
gion also recorded a lower abundance of non-forest and omnivorous Abundance of trees + 0.84 5 0.14
species (Appendix E). Several variables influenced the richness and Cattle pasture +
abundance of birds in cocoa agroforestry sites, but landscape composi­ Region
Cattle pasture + 1.17 4 0.12
tion had a stronger effect (and significant in several cases; Fig. 2) than
Region
local variables (Table 1). Indeed, cocoa agroforestry located in more Abundance Abundance of cocoa 0.00 5 0.98
forested landscapes presented greater richness and abundance of trees + Cattle pasture
frugivorous birds, with a similar pattern obtained for the abundance of + Region
forest birds. We also found that the increased representation of cattle Forest- Richness Cattle pasture 0.00 2 0.36
pasture at the landscape level had a negative and significant effect on dependent Abundance of cocoa 1.75 3 0.15
richness and abundance of most bird groups evaluated (Fig. 2). In birds trees + Cattle pasture
particular, we observed lower richness and abundance of complete Abundance Canopy closure + 0.00 5 0.67
Forest cover + Region
community and insectivorous species, and lower richness of forest, non-
forest, frugivorous and omnivorous birds in agroforestry located in Non-forest Richness Cattle pasture 0.00 2 0.11
dependent Canopy closure + 0.40 3 0.09
landscapes dominated by cattle pastures. Our results also showed that
birds Cattle pasture
the amount of agroforestry cover present at the landscape level had a Canopy closure 0.51 2 0.09
weak effect on richness and abundance of understory birds, with only a Abundance of cocoa 1.15 3 0.06
significant negative effect on frugivorous species richness and non-forest trees + Cattle pasture
species abundance across studied sites. Region 1.33 3 0.06
Basal area + Cattle 1.41 3 0.06
We finally verified that local vegetation had a slight effect on un­ pasture
derstory birds. In fact, our finding demonstrated that the increase of Abundance of trees + 1.77 3 0.05
canopy closure drives a significant enhancement in the abundance of Cattle pasture
insectivorous birds in these agroforestry systems. Similarly, the abun­ Canopy closure + 1.92 4 0.04
Region
dance of non-forest species increased in agroforests composed by higher
Abundance Abundance of cocoa 0.00 5 1
number of cocoa trees (Fig. 2; Appendix C). trees + Cocoa
agroforestry +
4. Discussion Region

Frugivorous Richness Cattle pasture 0.00 2 0.18

Although several studies have reported that agroforestry systems can birds Forest cover 1.25 2 0.1
help maintaining biodiversity in human-modified landscapes (Perfecto Cocoa agroforestry 1.41 2 0.09
Abundance Abundance of cocoa 0.00 5 0.43
et al., 1996; Faria et al., 2006; Clough et al., 2009), our findings indi­
trees + Forest cover +
cated that the surrounding landscape context is crucial to determine the Region
extent of their contribution for bird conservation. Five observed patterns Abundance of cocoa 0.63 3 0.31
deserve special attention. First, the highly disturbed region, which trees þ Forest cover
presents low amount of both forest cover and agroforestry, and is mostly Insectivorous Richness Abundance of trees + 0.00 3 0.19
dominated by pastures, harbored a more simplified bird community. birds Cattle pasture
Second, forest amount at the landscape scale positively influenced bird Canopy closure + 0.07 3 0.19
Cattle pasture
communities, mainly for those species that depend on certain resources
Cattle pasture 0.29 2 0.17
provided by forest patches, such as forest-dwelling birds and frugivores. Abundance of cocoa 1.77 3 0.08
Third, cocoa agroforests located in landscapes dominated by cattle trees + Cattle pasture
pasture hosted low diversity - richness and abundance - of bird assem­ Abundance Canopy closure + 0.00 3 0.52
blages, regardless of the evaluated ecological group. Fourth, increasing Cattle pasture

representation of shade plantations at landscape hardly buffered the Omnivorous Richness Region 0.00 3 0.12
species decline observed in deforested landscapes. Finally, local vege­ birds Cattle pasture 0.20 2 0.11
Basal area + Cattle 1.15 3 0.07
tation structure showed only a slight effect on understory birds,
pasture
although agroforests presenting a more closed canopy and a greater Abundance of trees + 1.17 4 0.07
number of cocoa trees showed a greater abundance of insectivores and Region
non-forest birds, respectively. We thus discuss possible mechanisms by Basal area + Region 1.61 4 0.06
which the environmental predictors are shaping understory bird com­ Canopy closure + 1.65 3 0.05
Cattle pasture
munities in cocoa agroforestry systems, and suggest some actions for
Abundance Basal area + Cocoa 0.00 5 0.77
bird conservation in these agricultural landscapes. agroforestry + Region
According to our predictions, we observed impoverished bird as­
ΔAICc: difference in AICc between the best model and the ith model; k:
semblages - at community level and for some ecological groups,
parameter number of the model; Wi: AICc weight. Models are ranked by AICc
including non-forest and omnivorous birds - in the highly deforested
values.
region, composed by small and isolated forest patches, commonly

5
J.P. Cabral et al.
Fig. 2. Effects of several environmental predictors estimated in the landscape and local scales on richness and abundance of understory birds in 18 cocoa agroforestry
systems. Blue and red boxes represent significant positive and negative effects, respectively. For more details, see Appendix C. (For interpretation of the references to
color in this figure legend, the reader is referred to the web version of this article.)
surrounded by a harsh matrix (i.e. cattle pastures), with low amount of
cocoa agroforestry. These landscape features are expected to act as
important environmental filters selecting bird species with low habitat
specificity (Julliard et al., 2006; Ekroos et al., 2010), and therefore
leading to biotic homogenization. Indeed, only six species were exclu­
sively recorded in the LFC region (Appendix F), indicating that species
composition is very similar to other sampled regions. In addition,
agroforests inserted in this disturbed region are likely to provide limited
resource availability for bird species, hence harboring more simplified
communities. Also, dispersal limitation imposed by pasture matrix can
prevent species from reaching resources available in small and already
scarce forest patches. In fact, several studies documented that forest
cover amount is a key predictor for structuring bird communities in
shaded plantations, such as cocoa agroforestry systems (Faria et al.,
2006; Clough et al., 2009; Schroth et al., 2011; Tscharntke et al., 2012).
Of particular importance, we showed that landscape composition
was a stronger driver than local vegetation structure for predicting bird
communities in the studied cocoa agroforests. Although the best models
included local variables as predictors of bird diversity, in most cases only
landscape features exerted a significant effect on richness and abun­
dance of birds (Appendix C). In concordance with our hypothesis,
agroforests located in more forested landscapes harbor greater richness
and abundance of frugivores and forest-dwelling birds. Forest cover has
been widely recognized to be a pivotal driver of biodiversity patterns in
human-modified landscapes, especially because this predictor is posi­
tively related to habitat amount and landscape connectivity for a wide
range of species, particularly forest species (Fahrig, 2003). For instance,
several studies documented that cocoa agroforests adjacent to forests
present higher bird diversity, including frugivorous, because species
that use these systems can obtain vital resources for their life cycle, such
as food, nesting sites, shelters and reproductive partners, in forest
remnants (Faria et al., 2006; Clough et al., 2009; Schroth et al., 2011;
Tscharntke et al., 2012). Also, a previous study performed in the same
region found higher fruit availability in more forested landscapes, key
resources positively affecting the diversity of forest frugivorous birds
(Morante-Filho et al., 2018). In fact, as frugivores depend on seasonal
resources, fruit scarcity in specific periods can be compensated by using
multiple habitats in the landscape (Hampe, 2008). More forested land­
scapes can facilitate species dispersion, mainly for forest birds, to obtain
a wide range of resources and foraging areas that are important to
ensure population persistence.
Considering that matrix quality highly mediates biodiversity
response in human-modified landscapes (Sánchez-de-Jesús et al., 2016;
Boesing et al., 2018; Shoffner et al., 2018), we expected a decrease in
6
Forest Ecology and Management 481 (2021) 118704
bird species richness and abundance in cocoa agroforestry systems
located in landscapes exhibiting greater representation of pastures
(Harvey et al., 2006). Our results clearly corroborated this hypothesis,
indicating a harsh effect of cattle pastures on all studied bird groups.
Specifically, open matrices, such as pastures, may represent hard bar­
riers limiting the movement of birds across the landscape (Boesing et al.,
2018), also increasing their risk of predation during dispersion (Biz
et al., 2017) and, thus, preventing the use of different habitats to supply
ecological requirements of species. Moreover, pastures can induce a
more severe edge effect on agroforestry, modifying microclimatic con­
ditions and hence generating a more adverse environment for birds,
especially those more sensitive to disturbances such as forest species and
insectivores. In accordance with the “landscape insurance hypothesis”
(Tscharntke et al., 2012), we suggest that the impoverishment of bird
assemblages in landscapes dominated by open areas (e.g. pastures) may
occur due to a reduction in the availability of complementary and/or
supplementary resources. Therefore, these overall rigorous conditions
imposed by cattle pastures act as key environmental filters, creating less
diverse bird communities in cocoa agroforestry systems integrated in
highly disturbed landscapes.
The increasing representation of agroforestry cover in the landscape
exerted only a slight, thought negative, effect on the abundance of non-
forest species and richness of frugivorous birds. Specifically, while non-
forest birds are well represented in cocoa agroforests (Faria et al., 2006),
these species are better adapted to use highly disturbed habitats.
Therefore, landscapes dominated by agroforestry systems can reduce the
availability of suitable habitats to support large populations of these
species. In fact, studies commonly reported a proliferation of non-forest
birds in landscapes presenting high land use intensification, mainly
composed by open agricultural areas (Goulart et al., 2013; Morante-
Filho et al., 2015; Kupsch et al., 2019). In addition, the low represen­
tation of frugivore species in these landscapes can be associated to
resource limitation imposed by cocoa agroforests. The fruits of the cocoa
trees can be consumed and even dispersed by some mammals, but rarely
used as a food item for birds (Clough et al., 2009), especially small-
bodied frugivores such as understory species. Although native shade
trees in this system bear fruits that are consumed by birds, tree diversity
– both richness and abundance - is significantly limited compared to
forests (Sambuichi, 2002), particularly in the understory which is
entirely replaced by cocoa trees (Clough et al., 2009). Therefore, local
vegetation simplification in cocoa agroforestry reduces fruit availability,
directly impacting frugivorous birds.
Although agroforestry intensification has been associated to local
species decline of birds (Clough et al., 2009; Harvey and Villalobos,
J.P. Cabral et al.
2007), we observed that local vegetation features indicating levels of
management intensification have a limited influence on understory
birds. Specifically, agroforestry systems characterized by many cocoa
trees and presenting more closed canopy showed a higher abundance of
non-forest and insectivorous birds, respectively. In particular, the local
increasing on the number of cocoa trees is a feature directly associated to
an increasing level of agroforestry intensification, a management prac­
tice that includes the removal of native shade trees to increase the
density of cocoa trees (Schroth et al., 2011). Therefore, management
intensification leads to local vegetation simplification, favoring the
proliferation of species adapted to open and disturbed environments,
such as non-forest birds (Kupsch et al., 2019). Conversely, plantations
characterized by more closed canopy, and thus a closer resemblance to
the original forest structure, can maintain more favorable environ­
mental conditions such as milder temperatures and greater availability
of resources, supporting more disturbance-sensitive species such as
forest-dwellers (Hansbauer et al., 2010). Indeed, 77% of insectivorous
birds recorded in our study are forest-dependent species (see Appendix
B) – a group commonly recognized for its high sensitivity to habitat
disturbances due to the low vagility and high dietary specificity
(Sekercioglu et al., 2002; Neuschulz et al., 2013). The increase of shade
levels enhances local conditions to host a larger diversity of potential
insect prey and foraging space, consequently attracting more members
of this functional bird group (Clough et al., 2009). Nevertheless, beyond
structural changes in local vegetation, intensification practices often
increase crop dependency on chemical inputs including herbicides and
broad-spectrum pesticides, practices with pervasive effects on the local
fauna, including bird species (Chang et al., 2018). Although not evalu­
ated here, it is noteworth that consumption of food items constantly
exposed to inseticides and herbicides in agricultural landscapes, such as
seeds, sprayed soils and prey arthropods, can additionally leads to
population declines of many bird species (Mineau and Whiteside, 2013;
Eng et al., 2017).
5. Conclusions
Although several studies documented the importance of agroforests
for the biodiversity conservation in agricultural landscapes (Perfecto
et al., 1996; Faria et al., 2007; Clough et al., 2009), our findings high­
lighted the overwhelming role of landscape features in which these
systems are integrated in shaping local bird diversity patterns. Rein­
forcing previous studies (Faria et al., 2006), we observed that cocoa
agroforestry systems can harbor a high diversity of birds, mostly
comprising forest-dwellers, when located in forested landscapes. How­
ever, when landscapes are dominated by cattle pastures, these systems
host impoverished bird communities, with lower diversity of both forest
and non-forest species. Interesting, this is the same pattern reported for
bird diversity in remnant forests, in which landscape-scale forest cover
strongly determined local diversity patterns, i.e. a significant decay in
local forest bird diversity was observed as deforestation levels increased
(Morante-Filho et al., 2015). Therefore, the persistence of forest-
dwellers in agroforests or forest patches in modified landscapes
strongly relies on a continuous influx of spillovers from surrounding
native forests (Tscharntke et al., 2008). Altogether, our results reinforce
the importance of native forest cover to guarantee the maintenance of
species diversity in tropical landscapes (Arroyo-Rodríguez et al., 2020),
even when landscapes comprise biodiversity-friendly land uses such as
cocoa agroforests. In addition, these shade plantations have a limited
contribution as bird diversity reservoirs in pasture-dominated land­
scapes, or even when they are the dominant land use.
This is an alarming result considering the current pace of tropical
deforestation - nearly four million hectares of tropical forest are lost
annually (Curtis et al., 2018), mainly for the implantation of agricultural
areas and cattle pastures. Unfortunately, this critical scenario is similar
for the Brazilian Atlantic Forest. During the period of 2018 and 2019, the
biome lost 14,500 ha, 27% more than in the last survey (2017–2018).
7
Forest Ecology and Management 481 (2021) 118704
Specifically, Bahia state lost 3,500 ha of Atlantic forest only in the last
year (Fundação SOS Mata Atlântica, 2020). Therefore, to guarantee the
effectiveness of agroforestry systems for bird conservation, we suggest
that farmers safeguard the existing forest remnants in their properties,
but also promote the expansion of forest cover in severely deforested
landscapes. In addition, in regions devoted to livestock production the
implantation of silvopastoral systems, which combine pastures with
native trees, can contribute to bird conservation, including forest-
dwelling species (Mastrangelo and Gavin, 2012). Based on our results,
we also recommend that large native trees should be maintained in
cocoa agroforestry to increase local shading, and specifically benefit
insectivorous birds, which are most sensitive and functionally important
species. This is particularly important given the increasing pace and
extention by which traditional agroforestry systems, that currently host
~60% of the regional carbon stocks (Schroth et al., 2015), are being
converted by thinning or even replaced by “full sun” plantations to
enhance local productivity (Schroth et al., 2011).
CRediT authorship contribution statement
Júlia Perez Cabral: Conceptualization, Data curation, Formal
analysis, Investigation, Writing - original draft, Writing - review &
editing. Deborah Faria: Conceptualization, Funding acquisition,
Writing - review & editing. José Carlos Morante-Filho: Supervision,
Conceptualization, Formal analysis, Funding acquisition, Writing - re­
view & 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.
Acknowledgements
We thank the reviewers and editor for all the suggestions and im­
provements on the manuscript. We thank Alana Cardoso, Albérico
Queiroz, Diego Flores, Fabrine de Almeida, Gabriela Burattini, Ilana
Araújo, Maísa Matuoka, Marcelo Souza and Sueli Damasceno for their
help in the fieldwork; and local landowners for allowing us to work on
their property. We also thank Goetz Schroth and Maíra Benchimol for
revision, Sérgio Lopes for helping to map the study area and FAPESB
(N◦ BOL0035/2018) for the financial support. This study was financed in
part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Su­
perior – Brazil (CAPES – Financing code 001) and the Instituto Nacional
de Ciência e Tecnologia em Estudos Interdisciplinares e Trans­
disciplinares em Ecologia e Evolução – INCT IN-TREE (CNPq-proc. n.
465767/2014-1, CAPES-proc. n. 23038.000776/2017-54).
Appendix A. Supplementary material
Supplementary data to this article can be found online at https://doi.
org/10.1016/j.foreco.2020.118704.
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