Landscape Ecol

https://doi.org/10.1007/s10980-019-00812-z (0123456789().,-volV)
(0123456789().,-volV)

RESEARCH ARTICLE

Divergent flows of avian-mediated ecosystem services

across forest-matrix interfaces in human-modified
landscapes
Fabio M. Barros . Carlos A. Peres . Marco A. Pizo . Milton Cezar Ribeiro

Received: 20 July 2018 / Accepted: 23 March 2019

Ó Springer Nature B.V. 2019

Abstract interfaces, and estimated their potential as pest

Context The ecological interplay between edge and control, seed dispersal and pollination agents across
matrix effects along forest-matrix interfaces is closed human-modified landscapes in southeastern Brazil.
linked to landscape processes modulating biodiversity Using Random Forest algorithm, we also quantified
and ecosystem services provision in disturbed land- the relative importance of local vs. landscape
scapes. Improving such knowledge is therefore essen- attributes in predicting ESPs.
tial to design more efficient land use management in Results The overall ESPs was higher in FP than FE
multifunctional landscapes. interfaces. Habitat generalist birds were important
Objectives Estimate the avian-mediated Ecosystem potential seed disperser and pollinator agents at both
Service Provision (ESP) in contrasting types of forest- FP and FE. At forest edges, landscape forest cover best
matrix interfaces in tropical landscapes, and examine predicted pest control services, whereas the density of
how local habitat and landscape attributes can predict rural homesteads best predicted potential seed disper-
ESPs. sal and pollination services. Local habitat features
Methods We sampled bird assemblages in forest- were particularly important in predicting all ESP in
pasture (FP) and forest-eucalyptus plantation (FE) pastures.
Conclusions We highlight the importance of matrix
type and matrix habitat structure in modulating avian
Electronic supplementary material The online version of ESPs across forest-matrix interfaces in human-altered
this article (https://doi.org/10.1007/s10980-019-00812-z) con- landscapes and suggest that forest cover and rural
tains supplementary material, which is available to authorized homestead density are key elements in multifunctional
users.
landscapes that consider avian ESP in both forest and
F. M. Barros (&)  M. C. Ribeiro matrix habitats.
Department of Ecology, São Paulo State University
(UNESP), Rio Claro, Brazil Keywords Cross-habitat spillover  Functional
e-mail: barros.fmon@gmail.com
traits  Forest cover  Rural homestead  Seed
C. A. Peres dispersal  Pollination  Pest control  Random Forest
School of Environmental Sciences, University of East algorithm  Pasture  Eucalyptus plantation
Anglia (UEA), Norwich, UK

M. A. Pizo
Department of Zoology, São Paulo State University
(UNESP), Rio Claro, Brazil

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Introduction Boesing et al. 2018), landscape-wide forest cover

(Banks-Leite et al. 2014), and landscape composition
Birds are involved in many ecological functions that and heterogeneity (Carrara et al. 2015; Lee and Martin
are essential for the maintenance of Earth’s ecosys- 2017) are important co-factors regulating bird persis-
tems (Sekercioglu et al. 2016). In both natural and tence in human-modified landscapes. However, the
anthropogenic habitats, birds provide direct and poorly understood interactions between edge effects
indirect ecosystem benefits to humans. In natural and matrix effects along forest-matrix interfaces is
ecosystems, birds often play a pivotal role in ecosys- also a crucially important ecological process modu-
tem functioning (e.g. via mutualistic and antagonistic lating bird persistence (Blitzer et al. 2012; Tscharntke
interactions), contributing to a balanced homeostasis et al. 2012; Boesing et al. 2018). The ability of birds
of healthy ecosystems (Sekercioglu et al. 2016). In and other organisms to spill over into neighbouring
croplands, avian insectivores enhance crop yields by habitat patches (hereafter, cross-habitat spillover) can
reducing pest abundance (Maas et al. 2016), particu- provide important cues on how forest species persist
larly in areas near forests (Karp et al. 2013) or within human-altered landscapes (Boesing et al.
embedded within forest landscapes (Boesing et al. 2018), enabling a better understanding of the conse-
2017). In fallow lands, avian seed dispersal agents quences of anthropogenic habitats on ecosystem
generate substantial seed shadows, accelerating regen- functioning and service provisioning (Tscharntke
eration trajectories and contributing to ecosystem et al. 2012).
resilience (Bregman et al. 2016; Carlo and Morales Several recent studies have examined the effects of
2016). Many tropical plant species are pollinated by land use intensification on avian foraging guilds. In
avian nectivores that can also act as important tropical regions, avian insectivores, frugivores and
pollinator agents in croplands (Sekercioglu et al. nectarivores have been singled out as most sensitive
2016). trophic guilds to land-use change compared to other
Although birds are essential in maintaining impor- functional groups (Sekercioglu 2012; Newbold et al.
tant ecosystem functions and services, they are often 2013; Bregman et al. 2016). Also, specialists of core
severely threatened by human activities. In tropical forest habitats are often replaced by habitat generalists
regions, habitat loss and fragmentation have been in highly disturbed habitats (De Coster et al. 2015;
considered the most important drivers of bird popu- Morante-Filho et al. 2015). However, little attention
lation declines (Haddad et al. 2015). Edge creation in has been given to the effects of landscape modification
tropical forests worldwide has severely contributed to on the strength of particular functions linked to ESP
edge-related bird declines (Pfeifer et al. 2017). (Luck et al. 2012). Although recent studies have
Understanding the ecological roles of rapidly prolif- provided valuable insights on how land use change
erating forest edges is critical, particularly considering affects avian-mediated ES (e.g. Muñoz et al. 2013;
that half of all remaining forest cover globally is now Bregman et al. 2016; Bovo et al. 2018; Morante-Filho
within 500 m of the nearest edge (Haddad et al. 2015). et al. 2018), none of them provide meaningful
This pervasive pattern of edge domination is aggra- quantification on avian-mediated ESP (Wenny et al.
vated in the once continuous [ 1.3 million km2 2011). Additionally, even less data are available on
Atlantic Forest biome (Muylaert et al. 2018), nearly patterns of cross-habitat spillover by bird communities
50% of which is now within 100 m from any edge in tropical forest-matrix boundaries (Blitzer et al.
(Ribeiro et al. 2009). Incorporating meaningful esti- 2012; Tscharntke et al. 2012; but see Boesing et al.
mates of context-specific ecosystem service provision 2018).
(ESP) (i.e. the benefits people obtain from ecosystems: In southeast Brazil, cattle pastures and eucalyptus
IPBES assessments, United Nations Environment monocultures are among the most dominant anthro-
Programme) can therefore be an important strategy pogenic matrix habitat types (Brockerhoff et al. 2012),
in achieving more efficient land use management and their relative importance to ESP by vertebrates
within fragmented forest landscapes (Sekercioglu remains poorly known (Sekercioglu et al. 2016).
et al. 2016). Although several studies have focused on the effects
In addition to the effects of anthropogenic edges, of tree plantations on bird communities, little is known
the matrix type (Kennedy et al. 2016; Biz et al. 2017; about the relative importance of eucalyptus

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plantations compared to other ubiquitous matrix types could be tolerant of external matrix habitats sharing
such as livestock pastures (Lindenmayer et al. 2008; similar vegetation structure, we expect that ESP by
de Camargo Barbosa et al. 2017). Here, we used diet- birds at forest-eucalyptus interfaces should be higher
related traits to assess differences on the potential flow than those at forest-pasture interfaces.
of three key ecosystem services (insect pest control,
seed dispersal and pollination) provided by birds
inhabiting forest-pasture and forest-eucalyptus inter- Methods
faces. We also examine which landscape and local
habitat variables can best predict avian-mediated ESP Study region
within three types of habitat edges (forest, pasture and
eucalyptus). Given that (1) eucalyptus plantations This study was conducted in a * 300,000-ha region of
typically retain tall trees and a fairly closed canopy, the state of São Paulo, southeast Brazil (W23°040 0900 ,
and provide lower structural contrast with adjacent S46°320 8700 ; Fig. 1), consisting of landscapes contain-
natural forests, and (2) birds inhabiting forest edges ing wide gradients of forest habitat loss and land use

Fig. 1 Study region showing the 32 bird sampling sites (black two examples of paired point-counts in forest-pasture (left) and
dots) surrounded by circular landscapes in southeastern Brazil forest-eucalyptus interfaces (right), both within 1.2-km radius
(2014–2015). The green patches and white background repre- circular landscapes classified according to land use types. The
sent native forest cover and the non-forest matrix, respectively. different colours represent different land use types. (Color
The inset higher-resolution landscapes (upper right) illustrate figure online)

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heterogeneity. The region was once entirely covered sampling sites were spaced by at least 2 km. To avoid
by the Atlantic Forest (Muylaert et al. 2018), but was potential spatio-temporal sampling biases (from an
subjected to intense resource exploitation leading to atypical annual climate, for instance), bird sampling
conversion of most natural vegetation into cropland, was spatially randomized across the entire study area
pastures and urban settlements (Morellato and Haddad in both sampling years (i.e. not restricted to a
2000). Most of the study area is currently comprised of particular portion of the study area at each sampling
cattle pastures and eucalyptus plantations (Eucalyptus year). Sampling landscapes were selected to ensure a
spp), with smaller areas of sugar-cane and other wide gradient of both forest cover (12–92%) and land
agricultural crops, including maze, citrus, and other use heterogeneity (Shannon diversity index; range
fruit cultivation. In contrast to vast areas dominated by 0.6–1.8).
large-scale mechanized farming elsewhere in Brazil,
our study landscapes are dominated by large numbers Quantifying avian-mediated ecosystem services
of smallholders and higher land-use heterogeneity
because of a more dissected topography (Oliveira and We developed three community-based metrics related
Fontes 2000). Natural vegetation in this region to the ability of bird assemblages to provide ecosystem
consists primarily of uneven-aged but mature services: pest control (PC), seed dispersal (SD) and
([100 years-old) secondary forest fragments of vary- pollination (PO). As such, we compiled dietary data
ing patch sizes (most of which are highly disturbed), (from Wilman et al. 2014) on the average proportion
wetlands and regeneration areas (i.e. abandoned lands of invertebrates, fruits and nectar consumed by each
in early successional stage). The Köpper’s climate bird species, which are used as proxies of potential
classification for the study region is Cwa (humid avian provision of pest control, seed dispersal and
subtropical with a dry winter and hot summer), and pollination services, respectively. For each species,
elevation ranges between 700 and 1700 masl (Oliveira the ESP value was therefore estimated as the species
and Fontes 2000). absolute local abundance multiplied by the percent-
ages of invertebrates, fruits and nectar in the diet. For
Sampling design each local species recorded, we define absolute
abundance the maximum number of individuals
Bird assemblages were recorded at forest-matrix recorded (seen or heard) among the three temporal
interfaces using 50-m fixed-radius point counts (Bibby repeats at each point-count site. At the assemblage
et al. 2002). We sampled birds within 16 forest- level, the ESP metric (in aggregate and for each ES)
eucalyptus and 16 forest-pasture interfaces, amount- was then calculated as the sum of ESP values for all
ing to 32 sampling landscapes across the study region. species sampled at each assemblage. These metrics
Each sampling landscape included two paired sam- likely provide meaningful estimates of the strength of
pling points, one within the forest edge and the other ecological functions and/or ES flows induced by any
within the adjacent habitat matrix (eucalyptus or given bird assemblage (Luck et al. 2012). We also
pasture). All paired sampling points were mirrored, computed the bird species richness (SR) for each
i.e. they were located 140–200 m apart from each sampling point within landscapes as the total number
other on opposite directions at 70–100 m from the of species detected.
forest margin (Fig. 1). All metrics aggregated for whole assemblages were
At each sampling point, we recorded any bird seen also examined for either forest specialist and habitat
or heard during 10 min per visit. Point-counts were generalist bird species. To do so, three highly expe-
repeated three times (amounting to 30 observation rienced field ornithologists provided scores based on
minutes per point) on different days from the onset of lifetime cumulative observations ([ 60 years in total)
sunrise to the first three daylight hours, amounting to a on levels of forest dependency for all bird species
total of 192 point-counts. All surveys took place detected [scores ranging from 0 (lowest) to 10
during two breeding seasons (15 paired point-counts (highest)]. These scores reflected the probability of
sampled from September 2014 to January 2015; and each species occurring within closed-canopy forest
17 paired point-counts sampled from October to environments. According to the field knowledge of the
December 2015). To minimize spatial autocorrelation, experts consulted, those species with average forest

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occupancy values ranging from 0.0 to 7.0 were defined connectivity (Bennett et al. 2006) and ecosystem
as habitat-generalists, whereas species scoring 7.1 or service provision by birds (Mitchell et al. 2013). Water
higher values were defined as forest-specialists. In any bodies are usually surrounded by wetlands or riparian
case, this threshold value produced a very accurate habitats that host high invertebrate abundance (Taft
classification on bird habitat preference according to and Haig 2005) and may also act as stepping stones or
field experts. foraging habitat for several bird species (mainly
insectivores and/or habitat generalists). These land-
Local and landscape predictors scape features may also favour avian ESP along forest-
matrix interfaces within agriculture-dominated land-
Two local variables were considered as predictors of scapes. We incorporated the percentage of silviculture
avian-mediated ESP: type of adjacent matrix and and pasture areas in the analyses because these matrix
habitat structure. While the first is a categorical types may regulate landscape connectivity for forest-
variable (pasture or eucalyptus), which was consid- specialist and generalist birds, respectively (de
ered only when sampling points were located within Camargo Barbosa et al. 2017), thereby influencing
forest sites, the latter was a simplified measure of ESP along habitat interfaces.
vegetation structure and other important local envi- To compute the landscape metrics, we first pro-
ronmental features that are known to affect habitat use duced land cover and land use maps within 1200-m
by birds (e.g. presence of regenerating vegetation in radial buffers from each forest sampling site using
eucalyptus, number of scattered trees in pastures, tree high-resolution images (ArcGIS 10.3 basemap ima-
density in forests). From the local habitat variables gery, DigitalGlobe satellites 2010–2011; scale of
sampled, we ran a principal component analysis 1:5000). To do so, we considered 14 land-use cover
(PCA) for each habitat type, wherein habitat structure classes (Fig. 1): forest, pasture, eucalyptus planta-
values were defined as the resulting scores from the tions, second-growth, wetland, cropland (mainly
first axis that best explained the total variation in the maze), sugar-cane, open-water, urban areas, rural
data (forest 55.2%, eucalyptus 59.9% and pasture homesteads, urban or suburban homesteads, paved
51.3%). Higher habitat structure values therefore roads, buildings, and bare soil. All ambiguous land
indicate overall higher structural complexity of matrix cover in terms of image interpretation were checked
habitats. Details on local habitat sampling and the and validated in the field. Once buffers were classified,
PCA analysis are provided in Supplementary Infor- we used Fragstats v.4 (McGarigal et al. 2012) to
mation S1. compute all landscapes metrics. We considered the
As landscape predictors, we considered seven 1200-m circular buffer size because it was the spatial
landscape variables: percentage of forest cover, edge scale (between 300 and 1200-m) that best explained
density, Shannon diversity index of the matrix mosaic, landscape predictors to bird richness and abundance
percentage of area under silviculture (i.e. Eucalyptus according to Random Forest algorithms (see Support-
plantation), percentage of pasture area, patch density ing Information S2).
of rural homesteads, and patch density of water bodies
(e.g. lakes and reservoirs). Edge density and Shannon Data analysis
diversity are frequently used proxies of landscape
heterogeneity (Fahrig et al. 2011). We defined rural We used pairwise t-tests to examine differences in
homesteads as small patches containing warehouses, ESP by bird assemblages between adjacent habitats
farmhouses, scattered trees, woodlots (including (forest-pasture and forest-eucalyptus), and Mann–
mainly exotic fruit trees), small ponds, cropland and Whitney tests to examine differences between non-
livestock facilities. We included this metric because adjacent habitats (forest-forest or pasture-eucalyptus).
rural dwellings typically cluster several key avian To assess whether species straddled the boundaries
resources (e.g. perches, nest sites, food) within between adjacent habitats, and the magnitude of ES
relatively small areas. Functioning as stepping stones potentially provided across forest-matrix interfaces,
between habitat patches or even suitable habitat for we computed the species richness and aggregate ESP
several bird species (mainly habitat generalists), these values for species recorded only in forest, only in the
dwellings are expected to facilitate landscape matrix (either pasture or eucalyptus), and in both

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habitats. To calculate aggregate ESP estimates, we simple estimators of variable importance (Cutler et al.
considered the incidence frequency, rather than the 2007; Crisci et al. 2012). Using regression trees, one
abundance, of all species throughout our study region can calculate the relative importance among a large
as a quantitative measure within each habitat type. For number of predictors and complex non-linear model
any given species using any two adjacent habitat relationships (Cutler et al. 2007; Triviño et al. 2011;
types, we were deliberately conservative by consider- Crisci et al. 2012). Moreover, this tool has a simple,
ing the lowest incidence frequency value across forest- intuitive interface, and can provide superior, or at least
matrix interfaces. comparable, predictive power compared to general-
To assess the relative importance of environmental ized linear models (GLMs) or other conventional
predictors of avian-mediated ESP, we used Random statistical modelling approach, even with small sample
Forest algorithm (randomForest package in R) (Cutler sizes (Cutler et al. 2007). All analyses were conducted
et al. 2007; Triviño et al. 2011; Crisci et al. 2012). We in the R environment, version 3.3.1 (R Development
ran 36 regression tree models, with nine predictor Core Team 2016).
variables (two local-scale and seven landscape-scale)
explaining four response variables (SR, PC, SD and
PO) within three habitat types (forest, pasture and Results
eucalyptus). Each model contained seven predictor
variables, six of which (habitat structure, forest cover, In total, we recorded 200 bird species across all 32
edge density, Shannon diversity, water bodies and sampling landscapes (64 paired point counts), 83.5%
rural homesteads) were included in all models, of which were found in forest edges, 52.2% in
whereas type of adjacent habitat, pasture cover and pastures, and only 24.5% in eucalyptus plantations.
eucalyptus cover were included only in the forest, From all species detected, 54% were considered as
pasture and eucalyptus models, respectively. forest-specialists and 46% as habitat-generalists. In
We used Random Forest algorithms to compute the terms of major dietary modes, 89% of all species
relative importance of predictors because they have consumed invertebrates, 50% fruits, and only 10%
been considered as the most powerful, accurate and floral nectar (mainly hummingbirds).

Table 1 Differences in the potential provision of ecosystem services by birds across ubiquitous forest-matrix interfaces in south-
eastern Brazil
All species ForP|Pas ForE|Euc ForP|ForE Pas|Euc

Species richness ?|– (**) ?|– (**) = (0.17) ?|– (**)

Pest control ?|– (**) ?|– (**) = (0.67) ?|– (**)
Seed dispersal ?|– (**) ?|– (**) = (0.15) ?|– (**)
Pollination =(0.14) ?|– (**) = (0.14) ?|– (**)
Forest specialists-
Species richness ?|– (**) ?|– (**) = (0.98) = (0.52)
Pest control ?|– (**) ?|– (**) = (0.94) = (0.59)
Seed dispersal ?|– (**) ?|– (**) = (0.68) ?|– (**)
Pollination ?|– (**) ?|– (**) = (0.66) = (0.48)
Habitat generalists
Species richness –|? (**) ?|– (**) ?|– (**) ?|– (**)
Pest control –|? (**) ?|– (**) ?|– (*) ?|– (**)
Seed dispersal = (0.18) ?|– (**) = (0.33) ?|– (**)
Pollination –|? (**) ?|– (**) = (0.48) ?|– (**)
ForP forest edges adjacent to pastures, ForE forest edges adjacent to eucalyptus plantations, Pas pasture edges adjacent to forest; Euc
eucalyptus edges adjacent to forest
(*) = P \ 0.05, (**) = P \ 0.001, (=) non-significant difference, (?) significantly higher values, (–) significantly lower values

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Cross-habitat spillover and avian-mediated ESP respectively, Table 1, Fig. 2). The total number of
forest-specialist species in the two forest edge types
Overall, ESP modulated by birds was significantly was similar (84 and 91 species in forests adjacent to
higher in forest sites than in either matrix types pastures and eucalyptus, respectively). However, the
(pasture or eucalyptus), except for pollination which overall bird richness restricted to forest edges (i.e.
did not show significant differences across forest- those using only forest and not the adjacent matrix)
pasture interfaces (z = - 1.60, P = 0.10) (Table 1, was substantially higher in forests adjacent to euca-
Fig. 2). In general, there were no differences in mean lyptus (92 species) than in forests adjacent to pastures
ESP between the two types of forest interfaces (68 species) (Fig. 3).
(adjacent to pasture or to eucalyptus), except for Pasture sites exhibited significantly higher ESP
habitat-generalists which had higher species richness estimates than eucalyptus stands (Table 1, Fig. 2).
and pest-control potential in forests adjacent to Overall, birds shared higher levels of SR and ESP
pastures than those adjacent to eucalyptus across forest-pasture than across forest-eucalyptus
(z = - 2.87, P = 0.004 and z = - 2.11, P = 0.03, interfaces, especially in relation to habitat-generalist

Fig. 2 Species richness and potential ecosystem service landscapes in Brazil. Values are shown as means and standard
provision (ESP) by birds within forest-pasture (N = 16) and deviations. (Color figure online)
forest-eucalyptus interfaces (N = 16), across human-modified

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b Fig. 3 Species richness and the potential ecosystem services SD. Despite a marked variation, there was actually a
provision (pest control, seed dispersal and pollination) by birds gain of 48% (± 123.1%) in estimated pollination at
(all species, forest specialists and habitat generalists) in both
forest-pasture and forest-eucalyptus interfaces across human- pastures sites (i.e. higher mean values in pastures than
modified landscapes in the southeastern Brazil. Values indicate in adjacent forests). In contrast, there were consistent
the total ecosystem services provision (ESP) by species and substantial losses in ESP from forest to neigh-
restricted to a single habitat (forest, pasture or eucalyptus) or bouring eucalyptus plantations, in the order of 77.0%
straddling the boundaries between habitats. (Color
figure online) (± 6.9%), 82.8% (± 6.7%), 81.0% (± 14.9%), and
72.6% (± 17.5%) for SR, PC, SD and PO,
respectively.
seed dispersal vectors (Fig. 3). Eucalyptus plantations In general, forest-specialists provided higher over-
per se hosted very little or no unique ESP, which in all all contributions to ESP within forest sites, whereas
cases were provided by bird species that also used habitat-generalists provided higher contributions in
adjacent forests (Fig. 3). In contrast, pastures retained the adjacent matrix. However, both functional groups
a significant pool of locally-unique countryside provided similar seed-dispersal contributions within
species, but all of those were habitat-generalists forest areas, and in terms of SR and PC within
(Fig. 3). eucalyptus plantations (Table 2). At forest sites,
The mean rate of ESP loss from forest to pasture habitat-generalists provided an even higher
was 35.3% (± 22.6%, standard deviation) for SR,
35.1% (± 25.4%) for PC, and 35.4% (± 31.7%) for

Table 2 Local and landscape variables that best predicted potential provision of ecosystem services by birds at forest edges, pastures
and eucalyptus patches across human-modified landscapes in southeast Brazil

‘‘Prop’’ indicates the relative proportion of potential ecosystem services provided by forest-specialists and habitat-generalists. ‘‘% var
expl’’ refers to the percentage of variation explained by regression tree models performed with Random Forest algorithms
HAB local habitat, FC forest cover, RUR density of rural homestead patches, ED edge density, SHM Shannon diversity of matrix
mosaics, WAT density of water bodies

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b Fig. 4 The relative importance of local and landscape predic- matrix habitats examined here, eucalyptus monocul-
tors (different colours) on species richness and the potential ture had significant lower avian-induced ESP than
ecosystem service provision (pest control, seed dispersal,
pollination) by birds in forest edges, pastures and eucalyptus pastures. Moreover, the overall loss of ESP was almost
plantations across human-modified landscapes in southeastern twice higher from forest to neighbouring eucalyptus
Brazil. IncNodePurity values indicates the total decrease in node than from forest to neighbouring pastures. These
impurities averaged over all regression trees (i.e. higher values differences can be related primarily to local habitat
indicate higher predictive power). (Color figure online)
structure within these two matrix types and, in any
case, forest sites retained significantly higher levels of
ESP than either their adjacent eucalyptus or pastures
contribution than forest-specialists in terms of PO sites.
services (Tables 1, 2). Local habitat structure was a decisive determinant
of all ESP metrics at pasture sites (Table 2, Fig. 4).
Local and landscape effects on avian-mediated Given that both biotic and abiotic factors and prox-
ESP imity to water bodies are likely associated to resource
availability for habitat-generalist countryside birds in
Regression trees performed by Random Forest algo- man-made grazelands (Mahood et al. 2012), this likely
rithms showed a wide range of results, with the amount induced higher ESP values in pastures compared to
of variance explained ranging widely across models eucalyptus stands. Although frugivores may be unaf-
(Fig. 4, Table 2). At forest sites, overall forest cover fected by the spatial structure of tree cover in pastures
was the best predictor of SR and PC, whereas rural near primary forest edges in the Amazon (Lasky and
homesteads were the best predictor of SD and PO Keitt 2012), other studies have shown the importance
(Fig. 4, Table 2). Forest cover was also the best of relict features in pastures to countryside birds
predictor of all ESP provided by forest specialists at (Mahood et al. 2012). Intensively managed pastures
forest edges. In eucalyptus plantations, although (e.g. those lacking scattered isolated trees), for
models yielded very low amounts of variation instance, typically retain lower bird diversity than
explained (Table 2), metrics related to landscape neglected pastures supporting lower livestock densi-
heterogeneity—mainly Shannon diversity index— ties and containing higher structural complexity and
were the best predictors of all measures of ESP scattered clusters of trees and shrubs (Mahood et al.
(Fig. 4, Table 2). In pastures, local habitat structure 2012). Given that our sampling design excluded
was the best predictor of all ESP metrics. Considering intensively managed homogeneous cattle pastures,
habitat-generalists across all habitats, ESP was best the higher ESP estimates for pastures, mainly in terms
explained by rural homesteads, edge density, and of seed dispersal and pollination services, likely
Shannon index for matrix diversity. In particular, all applies primarily to pastures with some degree of
ESP induced by habitat-generalists along forest edges structural complexity.
was best explained by rural homesteads. Details of the The higher vegetation structural contrast between
Random Forest analysis, including all non-linear forest and pastures may contribute to the higher
relationships between predictor and response variables overall ESP values across these habitats compared to
are available in Supporting Information S2. forest-eucalyptus interfaces (Table 1). Forest edges
adjacent to open habitats are more exposed to sunlight,
favouring light-demanding plant species, such as
Discussion shrubs and pioneer trees (e.g. Cecropia spp.) (Watling
and Orrock 2010). A greater availability of fleshy
Cross-habitat spillover and avian-mediated ESP fruits and flowers (Oosterhoorn and Kappelle 2000;
Galetti et al. 2003) may attract frugivorous and
Forest environments are widely known to retain higher nectivorous birds and, consequently, facilitate higher
productivity and heterogeneity than structurally sim- provision of seed dispersal (Morante-Filho et al. 2018)
plified and highly managed anthropogenic habitats, and pollination services along these habitat interfaces.
such as pastures or tree plantations (Newbold et al. Apart from that, shorter distances between forest
2015). However, comparing the two dominant types of edges and pastures induce higher frugivore bird

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diversity (Pizo and dos Santos 2011), and this likely provide high ES interactions (Pizo and dos Santos
contributes to the higher levels of avian ESP at forest- 2011).
pastures boundaries. In general, habitat generalists were widely repre-
Bird assemblage responses to commercial tree sented as potential ES providers in both pasture and
plantations are relatively well investigated worldwide. eucalyptus patches (Table 2). Moreover, they were of
Tropical tree plantations may improve landscape comparable importance to forest-specialists at forest
connectivity to forest birds (Zurita and Bellocq sites in terms of seed dispersal and pollination services
2010; de Camargo Barbosa et al. 2017), and support (Table 2). Indeed, birds exhibiting wide habitat-
diversified bird assemblages (Volpato et al. 2010), breadth can be important seed dispersal agents,
provided that plantations are older, lightly managed actively accelerating tropical forest regeneration
and include at least some native vegetation (Millan (Carlo and Morales 2016), as well as important
et al. 2015). However, contrary to some of these providers of pest control services in farmland near
studies, our findings show low bird species richness forest fragments (Boesing et al. 2017). Due to their
within eucalyptus stands near forest remnants, with an relatively high abundance, ability to use a broad range
average of only 9 species per site (amounting to 49 of of habitat types, and move through both natural and
the 200 species across all sites), and forest-specialists anthropogenic habitats (Table 1, Fig. 3), habitat gen-
avoided this matrix type more frequently than we eralists can play a key role in ecosystem service
expected. Although we accounted for local habitat delivery across forest-matrix interfaces. Although
variation, this may occur because our eucalyptus seed dispersal services provided by forest-specialist
stands were cultivated primarily for commercial birds cannot be ecologically compensated by habitat-
exploitation, even-aged (4–6 years old), homoge- generalist birds (Morante-Filho et al. 2018), the latter
neous and largely lacked native understorey vegeta- can still be helpful in providing SD services across
tion. This is one of the most hostile scenarios for bird highly disturbed landscapes. We therefore reinforce
species richness within eucalyptus plantations (Millan that special attention should be given to relatively
et al. 2015). ubiquitous habitat-generalist birds and other organ-
Bird species composition in eucalyptus plantations isms, if the primary goal is to enhance ecosystem
is often a nested subset of species inhabiting quasi- services in highly degraded landscapes (Pizo 2007).
natural forests (Wethered and Lawes 2005). In addi-
tion to the dearth of resources available for birds, Local and landscape effects on avian-mediated
simplified eucalyptus stands would at best provide ESP
redundant resources, which are already available in
adjacent forests. This may explain the higher richness At forest edges, landscape-wide forest cover was the
of forest-specialists restricted exclusively to forest best predictor of SR and PC services by entire bird
sites adjacent to eucalyptus (92 species) compared to assemblages and of SR and all ESP by forest-affiliated
forests adjacent to pastures (68 species) (Fig. 3). A species (Table 2, Fig. 4). This is consistent with the
large number of forest-specialists was consistently influence of landscape-wide forest cover on bird
found in forest patches than in neighbouring eucalyp- persistence (Banks-Leite et al. 2014). However, given
tus. However, eucalyptus plantations could still serve that the vast majority of studies have not assessed the
to enhance habitat connectivity for forest-specialists landscape structure affecting birds exclusively at
(de Camargo Barbosa et al. 2017), despite their low forest edges, our results suggest that forest cover can
habitat value for most resident bird species. similarly affect both core and edge habitats in birds,
Although our results on ESP by birds in matrix particularly in terms of the species richness and
habitats are valid only for edges influenced by forest ecological functions performed by forest species.
fragments, similar ESP estimates could be much lower Although landscape metrics related to land use
than those reported here for large core areas of heterogeneity (edge density and Shannon diversity
homogeneous pastures and eucalyptus stands. The index) were the best predictors of species richness and
lack of natural vegetation or stepping stones typical of all ESP at eucalyptus plantations, the explanation
extensive homogeneous matrix areas is hostile to power of our models was too low and not sufficiently
diversified bird communities that could otherwise informative (Table 2). In contrast, rural homesteads

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were the best predictor of SD and PO services by entire Given the high complexity of ecological processes
bird assemblages, and the best predictor of all ESP by operating within our study landscapes, we were unable
habitat-generalists along forest edges. These results to account for important features related to ESP, such
suggest that, beyond landscape heterogeneity per se, a as (1) the quality of species-specific interactions
higher density by rural homesteads throughout an promoting the effective flow of ES, (2) any detrimen-
otherwise uniform landscape can enhance the land- tal ecosystem disservices provided by some species
scape connectivity for avian-mediated seed dispersal (e.g. seed dispersal and pollination of invasive and
and pollination services. The presence of scattered alien species; predation on natural enemies of agri-
trees and small woodlots, for example, likely offer cultural pests), and (3) the direct effects of bi-
important resources for many habitat generalist directional spillover patterns on ecosystem processes
species, including thrushes (Turdus spp.), tanagers from forest to matrix areas and vice-versa (Blitzer
(Tangara spp.), hummingbirds (mainly Eupetomena et al. 2012). Despite such limitations, however, we
macroura), and bananaquits (Coereba flaveola). believe that the metrics used here can be useful in
These species are both ubiquitous and highly abundant assessing wider patterns of ESP by vertebrate and
in open-habitat areas but also serve important func- invertebrate communities at larger spatial scales
tions as seed and pollen vectors in human-modified (Eigenbrod et al. 2010), where more accurate in situ
landscapes (Pizo 2007). field measurements would be too labour-intensive and
inefficient. A better understanding of the flows of
Conclusions ecosystem functions and services can inform manage-
ment strategies that enhance the overall resilience of
We have shown that the erosion of bird species in anthropogenic landscapes.
highly altered neotropical landscapes and, conse- Finally, our data brings further evidence regarding
quently, the ecosystem services inherently flowing conservation issues in land use management that
from their trophic interactions can be almost twice as augmenting (1) local habitat complexity within the
severe across forest edges when they occur next to wider habitat matrix, (2) landscape-scale forest cover,
commercially exploited eucalyptus plantations than and (3) elements such as rural homesteads that disrupt
under comparable settings next to cattle pastures. The the spatial homogenization typical of modern agricul-
habitat complexity of pastures (e.g. presence of relict tural landscapes will likely enhance avian-mediated
scattered trees) can also positively affect the potential ESPs, which can ensure the regeneration capacity and
provision of ecosystem services by birds, rather than multifunctionality of hyper-disturbed landscapes in
surrounding landscape attributes. In addition, ESP by the tropics.
birds along forest edges was most affected by forest
cover for forest-specialists, and nearby rural home- Acknowledgements FMB is grateful to Brazil’s Ministry of
Education (CAPES) for his Ph.D. studentship and FAPESP
steads for habitat-generalists. The prevalence of such (Fundação de Amparo à Pesquisa do Estado de São Paulo, Grant
rural homesteads in agricultural landscapes may Numbers 2013/19732-1, 2013/50421-2 and 2016/15376-4) for
positively disrupt spatial homogenization across all financial support. Danilo Freire assisted with statistical
otherwise monotonous farmland matrix vegetation, analyses. Instituto Florestal do Estado de São Paulo granted a
research permit (260108-009.965/2014) to work at Parque
thereby favouring infiltration of habitat-generalist
Estadual do Itaberaba. Field ornithologists Eduardo
birds that potentially provide pollination and seed Alexandrino, Fabio Schunk and Carlos Gussoni participated in
dispersal services. This can apparently contribute to a the expert survey. We are grateful to Júlia Assis and Instituto de
higher forest regeneration capacity (i.e. higher spatial Pesquisas Ecológicas (IPE) for logistic support during
fieldwork. MAP is supported by a research Grant from the
resilience) across highly disturbed and fragmented
Brazilian Research Council (CNPq). MCR thanks FAPESP
landscapes. Our results highlight not only the impor- (Process #2013/50421-2), CNPq (Processes #312045/2013-1;
tance of matrix type, its habitat structure and land- #312292/2016-3) and PROCAD/CAPES (Project
scape attributes in maintaining ES provision by birds #88881.068425/2014-01) for their financial support. We are
thankful for all the comments and suggestions by the
along forest-matrix interfaces, but also the need for
anonymous reviewers.
further studies quantifying the potential provision of
ES in anthropogenic landscapes.

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