Received: 11 November 2017 | Accepted: 28 August 2018
DOI: 10.1111/1365-2664.13283
RESEARCH ARTICLE
Landscape structure regulates pest control provided by ants in
sun coffee farms
Natalia Aristizábal | Jean Paul Metzger
Department of Ecology, University of São
Paulo, São Paulo, Brazil
Correspondence
Natalia Aristizábal
Email: nati.aristizabal1@gmail.com
Present Address
Natalia Aristizábal, , Gund Institute for
Environment, University of Vermont,
Burlington, Vermont
Funding information
The Brazilian National Council for Scientific
and Technological Development (CNPQ);
Coordination for the Improvement of Higher
Education Personnel (CAPES); São Paulo
Research Foundation (FAPESP), Grant/
Award Number: 2013/23457-6; Brazilian
Ministry of Education
Handling Editor: Owen Lewis
J Appl Ecol. 2019;56:21–30.
Abstract
1. Ants play a fundamental role in coffee pest control. Despite this, there is a lack of
understanding about how landscape configuration and composition regulate the
ecosystem service provided by ants in sun coffee farms within highly fragmented
landscapes.
2. We measured whether landscape structure influences ants’ ability to regulate cof-
fee berry borer (CBB) in sun coffee farms in Southeastern Brazil. Considering the
ecological interactions between ants and CBB at three different stages of pest
control (reduction of CBB presence, CBB infestation, and CBB bean damage), we
measured pest control among 10 landscapes that represented a gradual differ-
ence in forest and coffee cover. We manipulated ants through exclusion experi-
ments and tested whether interactions between ants and different landscape
structure metrics (distance to forest fragments, 2-km-level forest cover, and
300-m-level forest and coffee cover) influenced pest control.
3. The presence of ants reduced CBB presence and CBB damage by up to 40%. We show
how pest control service indicators change depending on the landscape level. The prob-
ability of CBB presence increased with expanding coffee and forest cover at the 300-m-
level but decreased at the 2-km-level. CBB infestation reduced further after 25 m from
forest edges, suggesting ants that provide these ecosystem services are adapted to ma-
trix conditions in sun coffee farms. Ants reduced CBB presence, CBB infestation, and CBB
damage in landscapes with at least 40% 2-km-level forest cover. Beyond this threshold,
there is a turning point for ecological processes involved in pest control.
4. Synthesis and applications. This is the first long-term branch-level exclusion experi-
ment to present strong evidence of ants as efficient providers of pest control in sun
coffee farms. We show how landscape structure modulates key ecological pro-
cesses involved in three different ant-CBB interactions that regulate CBB popula-
tions. Forest cover measured at different landscape levels yielded different results
for CBB presence, emphasizing the importance of multi-scale studies for landscape
management. Considering surrounding forest cover and crop proximity to forest
fragments in planning the spatial arrangement of coffee farms can thus both im-
prove pest control as well as contribute to biodiversity conservation.
KEYWORDS
ants, Atlantic Forest, coffee berry borer, coffee borer beetle, coffee farms, ecosystem
services, land-use change, pest control
wileyonlinelibrary.com/journal/jpe
© 2018 The Authors. Journal of Applied Ecology | 21
© 2018 British Ecological Society

22 | Journal of Applied Ecology
1 | I NTRO D U C TI O N
Humans have altered more than 75% of the Earth’s ice-­free land
(Verburg, Erb, Mertz, & Espindola, 2013), including at least 40%
of natural habitats transformed into agricultural landscapes (Foley
et al., 2011). Agricultural intensification alters landscape structure,
ecological processes, and species diversity, as well as the provi-
sion of ecosystem services (Cardinale et al., 2012; Folgarait, 1998;
Mitchell et al., 2015; Tscharntke et al., 2008). In agroecosystems,
changes in landscape composition or configuration may modify
ecological processes that regulate pest control, acting on the per-
sistence and movement of predators at the landscape level (Bianchi,
Booij, & Tscharntke, 2006; Boesing, Nichols, & Metzger, 2017). Land
conversion also increases isolation from native habitats and typically
decreases abundance and activity of crop pests’ natural enemies
(Karungi et al., 2014). Given the increasing tendencies of habitat loss
and the possible changes in community composition with land con-
version, it is fundamental to test the effects of extreme land-­use
change for monoculture agriculture in the provision of ecosystem
services; specifically, how pest control by mobile organisms is mod-
ulated by landscape structure changes.
Coffee agroecosystems benefit from several ecosystem services
(Classen et al., 2014; Jha et al., 2014). One of these services is the reg-
ulation of the world’s major coffee pest, Hypothenemus hampei Ferrari
(Coleoptera: Curculionidae) or “coffee berry borer” (CBB) (Vega,
Infante, Castillo, & Jaramillo, 2009). CBB is a coffee plant specialist,
where females bore through coffee berries to reproduce. The brood
then feed off coffee beans which reduces coffee’s quality, weight,
and yield (Vega et al., 2009). Although bored coffee berries are still
marketable, in Brazil alone, the world’s leading coffee producer, CBB
activity represents $215–358 million dollars loss per year (Oliveira,
Auad, Mendes, & Frizzas, 2013). Considering that, over 10 million
hectares of native habitat in the world have been transformed for cof-
fee crops (FAO, 2016), and that more than 100 million livelihoods de-
pend on coffee production worldwide (Bunn, Läderach, Ovalle Rivera,
& Kirschke, 2015; Fair Trade Foundation, 2012), the search for natural
control methods for CBB is fundamental for economic and conserva-
tion reasons (Jaramillo, Borgemeister, & Baker, 2006).
Among species known as natural enemies of CBB, ants stand out
because they are extremely abundant in tropical systems (Fernández,
2003; Hölldobler & Wilson, 1990), where coffee is best produced. In
the lab, ant colonies can efficiently remove adult CBB (Armbrecht &
Gallego, 2007; Larsen & Philpott, 2010) and predate on immature CBB
directly inside bored berries (Morris & Perfecto, 2016). Studies in tra-
ditionally grown shaded coffee agroecosystems show several general-
ist ant species defend coffee plants from CBB colonization (Gonthier,
Ennis, Philpott, Vandermeer, & Perfecto, 2013), and predate on CBB
(Bustillo, Cárdenas, & Posada, 2002; Philpott & Armbrecht, 2006).
Reduction of forest habitat and landscape heterogeneity, as well as a
decline in habitat quality, can lead to a decrease in richness of twig-­
nesting and leaf litter ants that provide pest control services (De la
Mora, Murnen, & Philpott, 2013; Perfecto & Vandermeer, 2002). On
the contrary, expansion of coffee crop area, which can be related to
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ARISTIZÁBAL and METZGER
landscape simplification, has sometimes been associated with an in-
crease in CBB removal by ants (De la Mora, García-­Ballinas, & Philpott,
2015). A better understanding of the effects of landscape change on
the ecological processes involved in ant-­mediated regulation of CBB
in monoculture sun coffee farms could reconcile higher yield coffee
production and forest conservation (Morris, Jiménez-­Soto, Philpott, &
Perfecto, 2018; Vandermeer & Perfecto, 2007).
Therefore, the fundamental goal of this study was to examine ant-­
mediated pest control in sun coffee farms across different landscape
conditions. Specifically, we tested whether proximity to a forest frag-
ment and the amount of forest and coffee cover at different landscape
levels modulates the regulation of CBB by ants. We did this in sun-­
exposed coffee farms by experimentally excluding ants from selected
branches during an entire coffee production season in Southeastern
Brazil. We measured three indicators of pest control in which ants
could possibly interact with and regulate CBB: (a) CBB presence: we
counted presence or absence of CBB per branch to test the ability of
ants to prevent CBB from colonizing coffee berries; (b) CBB infestation:
we measured the percentage of CBB in branches to test the capacity of
ants to impede CBB population growth once at least one coffee berry
had been colonized; and (c) CBB damage: we calculated the percentage
of spoiled coffee beans to test the ability of ants to prevent further
fruit damage by predating adult and immature CBB inside bored ber-
ries. We expected our response variables (CBB presence, CBB infes-
tation, and CBB damage) would be higher on ant-­excluded branches.
Furthermore, we predicted CBB presence, CBB infestation, and CBB
damage to decrease as proximity to forest fragments and forest cover
increased, and as coffee cover decreased. Hence, we presumed ants
would provide more pest control of CBB in landscapes with higher per-
centages of forest and in coffee crops near forest fragments.
2 | M ATE R I A L S A N D M E TH O DS
2.1 | Study area
Our study took place in Southeastern Brazil, in a coffee-­producing
region called Mogiana and Sul de Minas in the border between the
States of Minas Gerais and São Paulo (Figure 1, see Supporting
Information Figures S1 and S2a,b). Brazil produces around 35%
of the commercialized coffee in the world (USDA, 2015) and the
Mogiana and Sul de Minas region produces two-­thirds of it for two
main reasons. First, the region is a culturally traditional area for cof-
fee production since the expansion of the railroad system at the end
of the 19th century (EMBRAPA, 2018). Second, the region has ideal
conditions for coffee production with a subtropical highland climate,
annual mean temperatures between 19°C and 22°C, and altitudes
between 800 and 1,300 m (EMBRAPA, 2018).
Nearly 90% of the coffee in Brazil is produced as sun coffee
(Ricci, Araújo, & Franch, 2002) in an area expanding more than 2
million hectares (EMBRAPA, 2016). Within this region, we selected
10 independent landscapes following the procedures presented
in previous studies from the same region (see Boesing, Nichols, &
Metzger, 2017; Librán-­Embid, De Coster, & Metzger, 2017; Saturni,

ARISTIZÁBAL and METZGER
F I G U R E 1 Study region and
geographical location of the 10 landscapes
(2-­km-­radius)
Jaffe, & Metzger, 2016). These landscapes, or circular sample areas
of 2-­km-­radii, were composed of an agricultural matrix and Atlantic
Forest remnants. The Atlantic Forest is an endangered biome con-
sidered a biodiversity hotspot (Myers, Mittermeier, Mittermeier,
Da Fonseca, & Kent, 2000) and an important supplier of ecosystem
services regionally and globally (Ferraz et al., 2014; Joly, Metzger, &
Tabarelli, 2014). Unfortunately, only 12%–16% of its known distribu-
tion remains (Ribeiro, Metzger, Martensen, Ponzoni, & Hirota, 2009).
The 10 2-­km-­level landscapes varied gradually in their amount
of forest cover from 10% to 55% (Figure 1). The matrix in our land-
scapes was a heterogeneous mosaic dominated by coffee and pasture,
with some sugar cane and Eucalyptus production (see Supporting
Information Figure S1). In each landscape, we established three sites
with ant-­exclusion experiments except for one landscape that could
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Journal of Applied Ecology | 23
only have two sites for logistical restrictions (one of the farms was
abandoned and sold). Therefore, we had a total of 29 experimental sites
involving 17 different farms. We only used Coffea arabica varieties of
Catuaí and Catucaí, which are physiologically similar because Catucaí
is a cross from Catuaí. We controlled for type of soil and management
practices. Farms in the study applied similar herbicides, fertilizers, and
pesticides and harvested semi-­manually (except for one property—
which included three experimental sites—that harvested mechanically).
2.2 | Landscape metrics and site selection
We used high-­resolution satellite images from ArcGIS 10.3 basemap
imagery (2009–2011) with a reference scale of 1:5,000 and 1 m res-
olution to map the landscapes, classify and quantify land-­uses (see

24 | Journal of Applied Ecology
Supporting Information Table S1). Land-­use barely changed from
years of used satellite images (2009–2011) to the years in which we
executed our experiments (2014–2015). Nonetheless, during our
fieldwork, we actively revised and corrected land-­use classifica-
tions when needed. To prevent spatial overlap, we kept landscape
centroids at a minimum distance of 6 km. We analysed landscape
composition and configuration at two different levels: a 2-­km-­radius
level for each selected landscape and a 300-­m-­radius level around
each experimental site (details below). Land-­use in selected land-
scapes did not vary greatly in 1, 2, or 3 km-­radius. We chose a
2-­km-­radius as our landscape level because some ant species com-
monly disperse within this distance after nuptial flights (Hölldobler &
Wilson, 1990), and a 300-­m-­radius based on ant-­foraging distances
(Carrol & Janzen, 1973).
Using FRAGSTATS 4.2 (McGarigal, Cushman, & Ene, 2012), we
measured the following landscape metrics as explanatory variables:
distance from experimental sites to the nearest forest fragment,
2-­km-­level forest cover, and 300-­m-­level forest and coffee cover.
To select a representative range of these variables for our exper-
imental sites, we first analysed all pixels inside radii of 300 m for
each landscape to better understand the relationship between dis-
tance to forest fragments and amount of native forest cover around
coffee crops in this region (see Supporting Information Figure S3).
Controlling for coffee variety restricted the selection of experi-
mental sites, but ultimately our study design included a range of
distances to forest fragments (5–110 m), 2-­km-­level forest cover
(10%–55%), 300-­m-­level forest cover (2%–60%), and 300-­m-­level
coffee cover (5%–80%).
2.3 | Ant-­exclusion experiments
To test the role of ants in CBB control, we experimentally manipulated
the presence of ants in selected branches of coffee plants during
the 2014–2015 production season. We set up 10 ant-­exclusion
experiments (Gonthier et al., 2013) per experimental site, right after
the main flowering in October 2014 (before berries developed to
ensure absence of CBB). In each coffee plant, we randomly selected
two neighbouring branches with similar number of flowers, height,
and position, and arbitrarily assigned one as the treatment branch
(ant-­excluded) and the other as the control branch. We then manually
removed ants (if there were any) and isolated the branches by tying
away any other branch that could potentially come into contact. Next,
we spread Tree Tanglefoot Insect Barrier (The Scotts Company, LLC)
along 10 cm of the ant-­excluded branch after the first seven nodes,
counting from the tip to the base (see Supporting Information Figure
S2c). This physical barrier excluded any terrestrial invertebrates,
including ants. We visited each experimental site once a month to
maintain exclusion experiments until June 2015. We used monthly
visits to count on each control and ant-­excluded branch (a total of
580 branches) the number of ants seen during five minutes of active
observations and the number of coffee berries produced and bored.
We marked but did not manipulate control branches, except for a
dot of Tanglefoot that would not exclude ants but would control for
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ARISTIZÁBAL and METZGER
any effect of Tanglefoot on CBB (see Supporting Information Figure
S2d). We collected a few individuals of the frequent visitor ant
morphospecies seen in our experimental branches for genus-­level
identification.
2.4 | Pest control indicators: CBB presence/absence,
infestation, and bean damage
We considered three response variables, or indicators of CBB regula-
tion, to test different ecological processes where ants and landscape
structure could be decreasing the probability of CBB presence and
the percentages of CBB infestation and CBB damage. Bored berries
are left with a 2 mm diameter hole drilled by adult females that lay
their eggs inside the coffee beans (Damon, 2000). The presence of
CBB, referred from here on as CBB presence, was considered when
there was at least one bored coffee berry on a branch. Absence was
considered when none of the coffee berries on a branch had CBB.
The second indicator was the percentage of bored coffee berries
out of the total number produced per branch, or “CBB infestation.”
Finally, the third pest control indicator was the percentage rotten or
damaged of each bored coffee bean, referred from here on as “CBB
damage.” On our last visit in June 2015, right before farmers’ harvest
time, we collected all coffee berries in our experimental branches.
We then separated bored from non-­bored berries and opened all
bored berries. To calculate bean damage percentage or “CBB dam-
age,” we measured the length of the galleries made by CBB and di-
vided it by the length of the coffee beans inside each bored berry
(Jiménez-­Soto, Cruz-­Rodríguez, Vandermeer, & Perfecto, 2013).
2.5 | Data analyses
We removed from the dataset two experimental sites that did
not show evidence of CBB presence on any of the branches.
Consequently, we analysed a subsample that included all 10 land-
scapes, but only 27 (out of 29) experimental sites. To test the ef-
ficiency of ant-­exclusion experiments, we performed a paired t-­test
of ant-­activity between all control and all treatment branches. We
tested the collinearity among the explanatory variables [distance to
forest fragments, 2-­km-­level forest cover, and 300-­m-­level forest
and coffee cover] and found no significant correlation. Therefore,
all four explanatory variables were used in further analyses. To test
the effects of forest and coffee cover change in exclusion of ants
on each of the three response variables (CBB presence, CBB infesta-
tion, and CBB damage), we performed forward model selection using
Akaike Criterion Information (AICc). We used GLMM with a bino-
mial distribution, the “glmer” function, and a logit-­link function in the
“lme4” package (Bates, Mächler, Bolker, & Walker, 2015; Zuur, 2009)
in r version 3.2.3 (Development Core Team, 2018). We performed
model selection using the “dredge” function from the MuMIn pack-
age in r (Bartoń, 2018), starting with a full model that included sepa-
rate fixed effects from the interaction of ant-­exclusion (presence or
absence of ants in branches), all landscape metrics, and “ant-­activity”
(number of ants seen in five minutes at every visit). We selected

ARISTIZÁBAL and METZGER
equally plausible models with ΔAICc < 2 (see Supporting Information
Table S2). To represent our experimental design, we included three
random effects in all models: the landscape identity, the experimen-
tal site identity nested within the landscape, and the plant identity
nested within the experimental site. Percentages were calculated
internally in models with the “cbind” function.
3 | R E S U LT S
3.1 | Provision of CBB control by ants
We monitored 20,308 coffee berries from which 2,217 (c. 10%) were
bored (1,112 in ant-­excluded branches and 1,105 in control branches).
Across all 10 landscapes and 17 farms, 47% of the branches had CBB
presence (at least one bored coffee berry) from which 51% were in
ant-­excluded branches and 43% in control branches. There were 892
ants seen in control branches and 57 ants in ant-­excluded branches
during a total of 30 minutes observations (5 minutes × 6 visits).
The average “ant-­activity” (ants seen) in control branches and ant-­
excluded branches were 0.55 and 0.04, respectively (p < 0.0001,
see Supporting Information Figure S4). Frequent ant morphospecies
visitors in our experiments were identified to the genus level (see
Supporting Information Table S3). Ants reduced the probability of
CBB presence and the percentage of CBB damage up to 40%. Out of
the 2,078 bored berries we opened, coffee beans in ant-­excluded
branches had an average of 51% damage and control branches had
41% damage (see Supporting Information Figure S5).
3.2 | Presence or absence of CBB per branch
For the binary data indicating CBB presence, the “dredge” func-
tion ran 275 possible models and there were three indistinguish-
able models selected (ΔAICc < 2) (see Supporting Information
Appendix S1, Figure S6, Tables S2, S4). These three models included
as fixed effects the interaction of ant-­exclusion with 2-­km-­level
forest cover, 300-­m-­level forest cover, and 300-­m-­level coffee
F I G U R E 2 CBB presence final model representation (lowest AICc). CBB presence probability per branch in response to the interaction of
ant-­exclusion and (a) 2-­km-­level forest cover, (b) 300-­m-­level forest cover, and (c) 300-­m-­level coffee cover. Shaded areas between curves
show the interaction of exclusion experiment (ants presence/absence) and intensity of pest control provision. Shaded areas in yellow
represent where ants had positive effects and in black negative effects
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Journal of Applied Ecology | 25
cover. The probability to detect CBB presence was higher in ant-­
excluded branches and increased generally as 300-­m-­level coffee
cover increased (p < 0.001) and 300-­m-­level forest cover increased
(p < 0.001), and it decreased as 2-­km-­level forest cover increased
(p < 0.001, Figure 2a–c).
3.3 | Percentage of CBB infestation per branch
Out of the 275 models created with the “dredge” function for CBB
infestation data, there were three models selected as equally in-
formative (ΔAICc < 2). The three models included as fixed effects
the interaction of ant-­exclusion with 2-­km-­level forest cover and
distance to the nearest forest fragment (see Supporting Information
Appendix S2, Figure S7, Tables S2, S5). The percentage of CBB infes-
tation was higher in ant-­excluded branches. Ants provided more CBB
infestation control in landscapes with less than 40% 2-­km-­level for-
est cover and after 25 m from forest edges (p < 0.001, Figure 3a,b).
3.4 | Percentage of CBB damage per coffee bean
Model selection analysis from 275 possible models for CBB damage
directly in coffee beans predicted five models that included as fixed
effects the interaction of ant-­exclusion with 2-­km-­level forest cover
and ant-­activity (see Supporting Information Appendix S3, Figure
S8, Tables S2, S6). Reduction in CBB damage by ants was more
intense in landscapes with less than 40% 2-­km-­level forest cover and
decreased as forest cover increased (Figure 4a,b).
4 | D I S CU S S I O N
This study presents new evidence that ants regulate CBB popula-
tions in sun coffee farms and that landscape structure regulates
key processes involved in the provision of this ecosystem service.
As forest cover increases in 2-­km-­level landscapes, the probability
to detect CBB presence and the percentage of CBB infestation and
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26 | Journal of Applied Ecology ARISTIZÁBAL and METZGER

F I G U R E 3 CBB infestation final model representation (lowest AICc). CBB infestation percentage per branch in response to the interaction
of ant-­exclusion and (a) 2-­km-­level forest cover, (b) distance to the nearest forest fragment, and (c) ant-­activity. Shaded areas between
curves show the interaction of exclusion experiment (ants presence/absence) and intensity of pest control provision. Shaded areas in yellow
represent where ants had positive effects and in black negative effects

F I G U R E 4 CBB damage final model representation (lowest AICc). CBB damage percentage per bored coffee bean in response to the
interaction of ant-­exclusion and (a) 2-­km-­level forest cover and (b) total number of ants seen in 5-­minute visits. Shaded areas between
curves show the interaction of exclusion experiment (ants presence/absence) and intensity of pest control provision. Shaded area in yellow
represents where ants had a positive effect and in black a negative effect

CBB damage decreases. However, ants provide stronger CBB pres-
ence, CBB infestation, and CBB damage regulation in landscapes with
lower forest cover and at c. 40% forest cover in 2-­km-­level, this ant-­
mediated CBB reduction ceases. Ants’ ability to reduce CBB infesta-
tion intensifies beyond 25 m from forest edges. As coffee cover and
forest cover increases in 300-­m-­level landscapes, ants represent up
to 40% less CBB presence detectability.
4.1 | Proximity to forest fragments and pest control
by ants
Proximity to forest fragments typically enhances pest control ser-
vices, mainly due to spillover edge effects from forests adjacent ag-
ricultural areas (Boesing et al., 2017; Rand, Tylianakis, & Tscharntke,
2006). However, in Southeastern Brazilian sun coffee farms, ant-­
mediated CBB infestation control seems to increase as the distance
from forest fragments increases. These results indicate that inside
the coffee matrix ants are considerably important to prevent fur-
ther CBB infestation once they have established. Ant prey removal
rates were tested using sentinel caterpillar experiments in sun cof-
fee farms in Kenya and contrary to our findings, the probability
of pest removal decreased as distance to the forest fragment in-
creased, specifically after 25 m (Milligan, Johnson, Garfinkel, Smith,
& Njoroge, 2016). This could suggest there are different ecological
processes involved in the reduction of CBB infestation in Brazilian
sun coffee farms other than predation or prey removal by ants such
as non-­consumptive attacks or indirect chemical deterrence (Morris
et al., 2018). This could also indicate that ants receive higher pre-
dation pressures themselves near forest fragments (Librán-­Embid
et al., 2017) and hence are less able to reduce CBB infestation.
4.2 | Coffee cover and pest control by ants
CBB presence was partially explained by the amount of coffee cover
around a 300-­m-­level, as observed in other studies (Avelino, Romero-­
Gurdián, Cruz-­Cuellar, & Declerck, 2012; De la Mora et al., 2015).
The probability to detect CBB presence increased as 300-­m-­level
coffee cover increased, where ants reduced up to 40% CBB presence

ARISTIZÁBAL and METZGER
when there is more than 60% coffee cover. Accordingly, in a study
in Mexican coffee farms, ants removed more CBB as the number
of coffee plants increased (De la Mora et al., 2015). Avelino et al.
(2012) showed that increasing coffee cover raised the abundance of
CBB and other coffee pests in low-­shade coffee farms in Costa Rica.
Coffee expansion may offer more area for CBB colonization, but it is
also providing more opportunities for CBB removal by ants that nest
and forage in the coffee matrix.
Farmers indicated in interviews that the major source of CBB col-
onization is fallen bored berries not harvested in the previous year.
Most Brazilian farms in our study did not sweep between coffee
plants after harvesting to prevent fallen bored berries to propagate
new CBB populations. Perhaps, the bigger the area transformed into
coffee crops, the more bored berries that fall to the ground and the
more chances of CBB dispersing and colonizing. Thus, in 300-­m-­level
landscapes, ground-­foraging ant species that help prey on bored
fallen berries year-­round (Armbrecht & Gallego, 2007; Morris et al.,
2018) may be important to regulate CBB presence in sun coffee farms.
Two of the five models better explaining CBB damage also in-
cluded 300-­m-­level coffee cover as a predictive variable. There was
some evidence that ants reduce the percentage of CBB damage re-
gardless of the amount of coffee cover and this trend strengthened
as the coffee crop area grew. Altogether, in our study, coffee expan-
sion hinted at two effects of pest control services by ants: less CBB
presence and CBB damage. This could mean that some ant species
involved in preventing CBB colonization are also small enough to for-
age in CBB galleries. It seems that these ant species that adapt well
to the sun coffee matrix are dominating the local ant community.
4.3 | Forest cover and pest control by ants
The relationships among ants, pest control, and forest cover are
more complex and far more interesting than we had predicted. The
2-­k m-­level landscapes seem to have a threshold in pest control
provision around 40% forest cover. The probability of CBB presence
decreases with more forest area, but there is more CBB presence
detection in ant-­excluded branches only until this threshold. Also,
ant-­excluded branches have less CBB infestation in landscapes
with lower forest cover. Likewise, ants and 2-­k m-­level forest cover
are likely predictors of CBB damage prevention. Independently of
the processes behind the arrival of CBB, once a coffee berry is
colonized by CBB, and bigger natural enemies (such as birds) can
no longer predate it, ants become an even more important source
of pest control. Coffee berries had less CBB damage in landscapes
with lower forest area, but ants reduced bean damage only until
around 40% forest cover in 2-­k m-­level landscapes. To explain this
unexpected result, we suggest that above 40% forest cover the
community of species in the landscape shifts and predatory pres-
sures on ants increase. A study in sun coffee farms in Costa Rica
showed bird abundances were higher with more forest cover (Karp
et al., 2013), potentially increasing predation on ants. Particularly
for this study, in the Atlantic Forest, bird communities that could
be influencing ant populations, apparently recover and stabilize in
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Journal of Applied Ecology | 27
landscapes with >30%–35% forest cover (Banks-­Leite et al., 2014).
Interactions among different functional guilds, or natural enemies
with common prey, may have negative impacts on pest control in
landscapes with increasing complexity, or >25% semi-­natural habi-
tat (Martin, Reineking, Seo, & Steffan-­D ewenter, 2013). Thus, we
suggest that in our study ants’ regulation of CBB at the 2-­k m-­level
was an indirect response to insectivorous bird abundances and
predating pressures on ants.
Forest cover in 300-­m-­level was selected as an important pre-
dictor of CBB presence control by ants. Contrary to what we found
for forest cover at 2-­km-­level, the probability to detect CBB pres-
ence in the absence of ants increased as forest cover in 300-­m-­level
landscapes increased. This coincides with previous findings in
200-­m-­level studies (De la Mora et al., 2013) along with our expec-
tations because forest fragments generally offer habitat and other
resources to ants and natural enemies such as insectivorous birds
(Boesing et al., 2017). Throughout our entire field season, even be-
fore coffee berries were growing, we observed ants foraging and
nesting in the coffee matrix. The most commonly observed ant gen-
era in our study have been associated with human-­disturbed hab-
itats and are omnivorous generalists (Fernández, 2003). However,
ants involved in our experiments, and hence in pest control, may not
necessarily be forest-­dependent and that may be why 300-­m-­level
forest cover did not predict an association for CBB infestation or CBB
damage. On the other hand, 2-­km-­level forest cover predicted asso-
ciations for every response variable in our study (CBB presence, CBB
infestation, and CBB damage). Forest cover in larger landscape-­levels
may change the abundance and behaviour of other CBB predators,
such as birds spilling over from forest fragments into coffee farms
(Boesing et al., 2017; Kellermann, Johnson, Stercho, & Hackett,
2008). Hence, affecting ant communities and their provision of eco-
system services. We found conflicting CBB presence results associ-
ated with forest cover at the 300-­m and 2-­km levels. This highlights
the importance of considering multi-­scale studies to plan agricul-
tural landscapes. There are different ecological processes involved
at each level and different conservation decisions that could be de-
rived from them.
4.4 | Ants contribution to pest control
The most commonly observed genera in our experimental sites
were Linepithema, Pheidole, Solenopsis, Crematogaster, Camponotus,
Neoponera, and Brachymyrmex, which were also found to be linked
with coffee agroecosystems in previous studies (Armbrecht &
Gallego, 2007; Armbrecht & Perfecto, 2003; De la Mora & Philpott,
2010; Perfecto & Vandermeer, 2002). Ant species involved in the
suppression of CBB presence may not be the same as the species
that regulate CBB infestation or CBB damage. Presumably, the most
territorial species out of these genera would prevent more CBB
presence and CBB infestation and other smaller and arboreal or
ground-­foraging species would reduce more CBB damage. Out of
the ant genera commonly observed in our experimental sites, spe-
cies from Linepithema, Pheidole, and Solenopsis are small enough to
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28 | Journal of Applied Ecology ARISTIZÁBAL and METZGER

fit through CBB galleries and could potentially predate CBB inside AC K N OW L E D G E M E N T S
coffee berries. Individuals from the genus Solenopsis were found
We thank farm owners and workers for their fundamental
on several occasions inside bored coffee berries (authors’ obser-
cooperation. We would like to acknowledge Inara R. Leal and
vations). Evaluating CBB damage from field collected samples is
Sebastián F. Sendoya for their input on the experimental design
not typically utilized to quantify pest control. Using CBB damage
and contributions throughout this project. Also, we thank Carla
as an indicator of pest control was fundamental to better under-
R. Ribas and Paulo S. Oliveira for valuable discussions over the
stand this system. Pest control provided by arboreal and ground-­
first version of this manuscript, Gustavo Bravo for his support,
foraging ants is not restricted to preventing CBB colonization or
Danielle Rock for English revisions, and Sheina Koffler for
decreasing infestation. It also minimizes CBB damage directly in
help with statistical analyses. This study also benefitted from
coffee beans, which is ultimately what will profit farmers.
teamwork from all members of the Interface Project, particularly
from Guilherme Prata Gonçalves with ant identifications (SISBIO/
4.5 | Conclusion and management implications ICMBio permit 48059), and from Adrian Gonzalez, Elizabeth
Nichols, Francisco d’Albertas, Greet De Coster, Larissa Boesing,
Sun coffee is usually considered “low-­quality habitat” and sometimes
and Leandro R. Tambossi with assistance in spatial and statistical
even disregarded for ecosystem services. We show here that this is
analyses. Finally, we would like to thank assistance in the field,
not the case in Southeastern Brazilian sun coffee farms. This study
especially from Emilien Rottier. We are grateful to the São Paulo
highlights the significance of ants in pest control by reducing CBB
Research Foundation, which supported this study embedded
presence, infestation, and damage through their interaction with the
in funding for Interface Project (FAPESP, 2013/23457-­6). The
surrounding landscape. This is the first long-­term branch-­level ant-­
Brazilian Ministry of Education supported N.A. (CAPES-­DS;
exclusion study in sun coffee farms and it conveys new information
2014–2016). The Brazilian National Council for Scientific and
that allows us to propose useful landscape management recommen-
Technological Development funded J.P.M.
dations that could reduce CBB and increase coffee yield in one of
the world’s most economically important regions for coffee produc-
tion. These recommendations reinforce ecological CBB control while AU T H O R S ’ C O N T R I B U T I O N S
contributing to the protection of the endangered Atlantic Forest.
N.A. and J.P.M. conceived the project and wrote the manuscript.
Increasing forest cover by promoting forest restoration within pas-
J.P.M. obtained funding. N.A. collected and analysed the data.
ture areas and allocating forest near to coffee crops could lower the
probability of CBB presence. Guaranteeing 35%–40% of forest cover
in a 2-­km-­radius around coffee crops will maintain coffee branches DATA AC C E S S I B I L I T Y
with less CBB presence, CBB infestation, and CBB damage, while also
maintaining forest cover above extinction thresholds for several ver- Data available via the Dryad Digital Repository https://doi.
tebrates and plant groups from the Atlantic Forest (Lima & Mariano-­ org/10.5061/dryad.3rh2043 (Aristizábal & Metzger, 2018).
Neto, 2014; Martensen, Ribeiro, Banks-Leite, Prado, & Metzger,
2012; Pardini, Bueno, Gardner, Prado, & Metzger, 2010; Rigueira, da ORCID
Rocha, & Mariano-Neto, 2013).
We recognize CBB colonization is also affected by other fac- Natalia Aristizábal http://orcid.org/0000-0002-1001-8824
tors not tested in this study, such as farm management, humidity,
and local temperature. We advise incorporating these variables
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Additional supporting information may be found online in the
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How to cite this article: Aristizábal N, Metzger JP. Landscape
structure regulates pest control provided by ants in sun coffee
farms. J Appl Ecol. 2019;56:21–30. https://doi.
org/10.1111/1365-2664.13283