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How ants, birds and bats affect crop yield along shade gradients in tropical cacao agroforestry

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Tropical agroforests are diverse systems where several predator groups shape animal communities and plant–arthropod interactions. Ants, birds and bats in particular can reduce herbivore numbers and thereby increase crop yield. However, the relative importance of these groups, whether they interact, and how this interaction is affected by management and landscape context, is poorly understood. 2.We jointly manipulated access of ants, birds and bats in Indonesian smallholder cacao agroforestry across gradients of shade and distance to natural forest. We quantified arthropod abundance, pest damage and yield. 3.In control treatments, yield was highest under 30–40% canopy cover. Ant exclusion strongly reduced yield (from 600 to 300 kg ha−1 year−1) at 15% canopy cover. Bird exclusion impaired yield (from 400 to 250 kg ha−1 year−1) at 60% and enhanced yield (from 600 to 900 kg ha−1 year−1) at 15% canopy cover, while bats had no effect. Yield increased with forest proximity, a pattern not related to predator access. 4.No interactive effects among predator exclusions on yield, pest damage and arthropod communities were found. Ant exclusion increased numbers of herbivores below 30% canopy cover, without reducing spider abundances. Bird exclusion reduced herbivore and increased spider abundances. 5.Synthesis and applications. Using exclusion studies, we estimated that ants and birds cause cacao yield to vary between 100 to 800 kg ha−1 year−1, depending on shade-tree management. In all but the most shaded agroforests, ants were pivotal in supporting yields. Yields under low-canopy cover were strongly dependent on access by predator groups, with birds reducing rather than increasing yield. Hence, cacao farmers should refrain from disturbing ant communities and maintain 30–40% shade-tree canopy cover not only for ecophysiological reasons but also to buffer variability in predator communities. This article is protected by copyright. All rights reserved.
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How ants, birds and bats affect crop yield along shade
gradients in tropical cacao agroforestry
Pierre Gras
1,
*, Teja Tscharntke
1
, Bea Maas
1,2
, Aiyen Tjoa
3
, Awal Hafsah
3
and Yann Clough
1,4
1
Agroecology, Georg-August-Universit
at G
ottingen, G
ottingen, Germany;
2
Division of Tropical Ecology and Animal
Biodiversity, Department of Botany and Biodiversity Research, University of Vienna, Vienna, Austria;
3
Fakultas
Pertanian, Universitas Tadulako, Palu, Indonesia; and
4
Centre for Environmental and Climate Research, Lund
University, Lund, Sweden
Summary
1. Tropical agroforests are diverse systems where several predator groups shape animal com-
munities and plantarthropod interactions. Ants, birds and bats in particular can reduce her-
bivore numbers and thereby increase crop yield. However, the relative importance of these
groups, whether they interact, and how this interaction is affected by management and land-
scape context, is poorly understood.
2. We jointly manipulated access of ants, birds and bats in Indonesian smallholder cacao
agroforestry across gradients of shade and distance to natural forest. We quantified arthro-
pod abundance, pest damage and yield.
3. In control treatments, yield was highest under 3040% canopy cover. Ant exclusion
strongly reduced yield (from 600 to 300 kg ha
1
year
1
) at 15% canopy cover. Bird exclusion
impaired yield (from 400 to 250 kg ha
1
year
1
) at 60% and enhanced yield (from 600 to
900 kg ha
1
year
1
) at 15% canopy cover, while bats had no effect. Yield increased with for-
est proximity, a pattern not related to predator access.
4. No interactive effects among predator exclusions on yield, pest damage and arthropod
communities were found. Ant exclusion increased numbers of herbivores below 30% canopy
cover, without reducing spider abundances. Bird exclusion reduced herbivore and increased
spider abundances.
5. Synthesis and applications. Using exclusion studies, we estimated that ants and birds cause
cacao yield to vary between 100 and 800 kg ha
1
year
1
, depending on shade-tree manage-
ment. In all but the most shaded agroforests, ants were pivotal in supporting yields. Yields
under low-canopy cover were strongly dependent on access by predator groups, with birds
reducing rather than increasing yield. Hence, cacao farmers should refrain from disturbing
ant communities and maintain 3040% shade-tree canopy cover not only for ecophysiological
reasons but also to buffer variability in predator communities.
Key-words: agricultural intensification, biocontrol, canopy cover, ecosystem services, forest
distance, mesopredator release, predation, Theobroma cacao, trophic interactions, yield
Introduction
Predators exert top-down control and can positively or
negatively influence plant development through direct and
indirect interactions affecting pests and diseases (Vander-
meer et al. 2002; Vandermeer, Perfecto & Philpott 2010).
Detailed reviews covering effects of ants, birds and bats
on arthropod communities and crop yield, often assessed
using exclusion experiments, underline their importance
for ecosystem service provision (Philpott & Armbrecht
2006; Van Bael et al. 2008; Whelan, Wenny & Marquis
2008; Mooney et al. 2010; Kunz et al. 2011; Wenny et al.
2011; Maas et al. 2015b).
Ants are effective biocontrol agents, especially in tropi-
cal agroforestry. For example, in Mexican coffee arboreal
ants protect trees from colonization by important pests
(Gonthier et al. 2013). However, impacts of ants depend
on the environmental context (e.g. temperature), ant
species involved (Philpott & Armbrecht 2006; Gove 2007;
Wielgoss et al. 2014), potential counterproductive effects
*Correspondence author. Department of Crop Sciences, Agroe-
cology, Georg-August-Universit
at G
ottingen, Grisebachstr. 6,
37077 G
ottingen, Germany. E-mail: pgras@gwdg.de
©2016 The Authors. Journal of Applied Ecology ©2016 British Ecological Society
Journal of Applied Ecology 2016 doi: 10.1111/1365-2664.12625
on mesopredators such as spiders (Eubanks 2001), mutu-
alism and plant-sucking trophobionts (i.e. aphids and
mealbugs) that are harmful to crops. Birds have also been
shown to reduce abundances of pests (Holmes, Schultz &
Nothnagle 1979; Johnson et al. 2009), with yield losses
up to 310 kg ha
1
year
1
prevented in coffee agroforestry,
for example (Karp et al. 2013). Effects of birds on
arthropod communities are not always that strong, can
negatively affect mesopredators and do not necessarily
trickle down to plants (Williams-Guill
en, Perfecto & Van-
dermeer 2008; Maas, Clough & Tscharntke 2013). Bats
have received increased attention as biocontrol agents in
recent years following several seminal reports from natural
forests and agroforests (Kalka, Smith & Kalko 2008; Wil-
liams-Guill
en, Perfecto & Vandermeer 2008). Efforts to dis-
entangle bird and bat effects have partly confirmed the
potential of bats as biocontrol agents in agroforestry
(Maas, Clough & Tscharntke 2013; Maas et al. 2015b) and
partly suggested that negative impacts on spiders can can-
cel out the effects that bats may have on herbivores (Karp
&Daily2014).
Effects of these predator groups have usually been con-
sidered in isolation, using exclusion experiments con-
ducted in only one or a handful of locations. In reality,
density and diversity of predators, and thus probably also
their biocontrol effect, depend on local management or
landscape context (Clough et al. 2009; Karp et al. 2013).
In addition, it is unclear whether impacts of the three
predator groups are complementary or redundant. Few
studies have tested interactive effects (but see Mestre
et al. 2013b; Mooney 2007; Pi~
nol et al. 2010; Philpott
et al. 2004; Spiller & Schoener 2001). Finally, few studies
quantify impacts on crop yield, making economic assess-
ments difficult since plants can often compensate for
damage (but see Mooney et al. 2010; Wielgoss et al.
2014; Maas, Clough & Tscharntke 2013; Karp & Daily
2014).
Here, we simultaneously investigate effects and manage-
ment dependency of ant, bird and bat exclusions in 15
smallholder cacao plantations differing in the percentage
of shade-tree canopy cover and distance to forest margins.
In our study region, Central Sulawesi (Indonesia), results
from separate experiments revealed that both ant and
combined birdbat exclusions decreased yield by ~30%
(Maas, Clough & Tscharntke 2013; Wielgoss et al. 2014).
These effects may change along canopy cover gradients as
local shade-tree management impacts productivity, fruit
abortion, and arthropod and vertebrate communities
(Bos, Steffan-Dewenter & Tscharntke 2007a; Clough et al.
2009). Increasing distance from natural forest can also
negatively affect the density and diversity of bird and bat
communities, and therefore the degree of biocontrol
(Estrada & Coates-Estrada 2002; Clough et al. 2009). In
the present study, we addressed the following questions:
1. Does exclusion of ants, birds and bats affect cacao
yield, and if so, does this change with shade-tree canopy
cover or distance to forest margin?
2. Are effects of the three manipulated predator groups
synergistic, additive or antagonistic?
3. What are the likely processes explaining impacts
of ant, bird or bat exclusions on cacao crop yield,
pest and disease infestation, and fruit set or fruit
abortion?
4. What are the management implications for cacao farm-
ers in terms of canopy cover, landscape-scale forest
preservation and predator conservation?
Materials and methods
SITE SELECTION AND GRADIENTS
Fifteen smallholder Theobroma cacao L. plantations were selected
at the eastern border of the Lore Lindu National Park in Central
Sulawesi, Indonesia (Fig. 1; 1°230318S 120°1805755E, ~1130 m
a.s.l., 19903804 mm rainfall) to cover five distances to the forest
margin (Fig. S1, three agroforests in each category: 0250, 251
500, 5011500, 15012500, 25013000 m) and three canopy cover
types (Fig. S1, five agroforests in each category: <30%, 3050%,
>50%). Later, both variables were measured in metres to the for-
est margin or percentage of shade-tree canopy cover. The latter
was measured at the experimental treatment level (within agro-
forest), but variability was larger between than within agro-
forests. Local farmers managed all agroforests and we
incorporated pesticide-, herbicide- and fungicide-free areas to
minimize management differences. Nonetheless, each agroforest
provided a unique habitat due to agroforest size, cacao tree age/
abundance, previous/nearby land-use, topography, drainage, fer-
tilizer use (Table S18) or intercropped vegetables and fruits
(Tables S2 and S3). The agroforests were separated by at least
500 m edge-to-edge distance. Two planted legume shade-tree spe-
cies Erythrina subumbrans Merr. and Gliricidia sepium Kunth
represented 3091% of all recorded non-crop trees (Table S2,
herb species in Table S3). We trimmed the herb layers every
2 months using a motor scythe. During the experiment, we
recorded 49 ant and 69 bird species (Tables S4S6).
EXCLUSION TREATMENTS
Bird and bat exclusions were implemented in 2010 (cf. Maas,
Clough & Tscharntke 2013), and ant exclusions were added in
April 2011; both were maintained until June 2012. Exclusions con-
sisted of eight randomly positioned treatments (two trees each)
per study site: (i) no exclusion, (ii) ant exclusion, (iii) bird exclu-
sion, (iv) bat exclusion, (v) antbird exclusion, (vi) antbat exclu-
sion, (vii) birdbat exclusion and (viii) antbirdbat exclusion.
We used bamboo scaffolds covered with fishing nets
(35 935 mm mesh size) to exclude birds and/or bats. The bird
bat exclusion treatments had fixed nets. Bird exclusion nets were
manually opened in the morning (05:30 h) and closed in the eve-
ning (18:30 h), while bat exclusions were opened in the evening
(18:30 h) and closed in the morning (05:30 h). Controls were
always open. Open nets (top and all sides) were bound tightly to
the scaffolds (Fig. S7). To exclude ants, we used cone-shaped
insect glue rings fitted to the tree trunks (Fig. S8), thereby reduc-
ing contact between ring and trunk and preventing trunks from
getting mouldy a problem encountered while planning a previ-
ous study (Wielgoss et al. 2014). Thus, ant exclusion effects are
©2016 The Authors. Journal of Applied Ecology ©2016 British Ecological Society, Journal of Applied Ecology
2P. Gras et al.
similar to conventional insect glue applications. We destroyed ant
nests during establishment of ant exclusions, whenever discovered
and during a monthly ‘search-and-destroy’ survey. Arthropod
exchange through nettree contact was avoided by regularly
pruning branches to keep at least 30 cm between foliage and
nets/scaffolds. Effectiveness of ant exclusion was quantified by
counting ant individuals from canopy knock-down fogging sam-
ples, showing that ant abundance was strongly reduced (by 60
90%, see Results) in exclusions compared to control treatments.
SAMPLING AND SURVEYING METHODS
We obtained distances to forest margins and agroforest area
using a Garmin Oregon 550 Global Positioning System device
(Fig. 1). We took treatment-level digital hemispherical canopy
photos and calculated percentage of canopy cover using the
CIMES-FISHEYE software (Walter 2009). We measured several
potentially yield-related covariates: (i) cacao tree crown volume
and (ii) mean d.b.h. to represent tree size, (iii) daily mean temper-
ature and (iv) precipitation to represent abiotic conditions, (v)
non-crop tree richness known to correlate with the bird commu-
nity composition (Clough et al. 2009), (vi) the average branch
perimeter as indicator of fruit carrying capacity and (vii) the pod
groove depth which indicates ‘on-fruit’ hiding opportunities for
arthropods and can differ between agroforests depending on the
cacao phenotype (Tables S9 and S10).
Every 2 weeks from April 2011 to May 2012, we surveyed all
experimental trees counting and classifying cacao fruits by size/
development and presence/absence of pest and disease symptoms
and harvesting of ripe fruits (classification details, Tables S11
and S12). We separately quantified the weight of marketable
and damaged beans (i.e. due to the damage of the cacao pod
borer Conopomorpha cramerella). Damage caused by the most
economically important organisms (i) C. cramerella, (ii) Helopel-
tis sulawesi and (iii) Phytophthora palmivora was assessed by
counting fruit with symptoms of damage.
We recorded other pests damaging leaves, flowers and fruits
(e.g. aphids, herbivorous bugs and caterpillars), as well as meso-
predators (e.g. spiders, earwigs and lacewing larvae) through
canopy knock-down fogging with a mixture of 5% Malathion
(Fumithion 1150 ULV) and diesel fuel (Bos, Steffan-Dewenter &
Tscharntke 2007b; Rizali et al. 2013) at the end of the experi-
ment. We fogged all treatments (covered by plastic tents) for
5 min and left the tents closed for 1 h. Fogging samples were
used to test predator exclusion effects on arthropod orders.
Every 4 weeks from May 2011 to March 2012, ants were baited
on trees without ant exclusions to detect effects of shade/forest
distance on ant community abundance, richness and composition.
We used protein (tinned tuna in brine) and carbohydrate (satu-
rated sugar solution) baits. We identified ant/morphospecies using
taxonomic literature (Bolton 1994; Fisher 2010) and regional ant
collections (Rizali et al. 2013; Wielgoss et al. 2014).
Between September 2010 and June 2011, the bird community
was recorded by repeated mist netting surveys and point count
recordings on all 15 study sites (see Maas et al. 2015a for details).
STATISTICAL ANALYSES
Data from 28 harvests were summed for each agroforest and
treatment. Response variables directly related to yield (total mar-
ketable yield, fruit abundance and fruit weight) were analysed in
three steps. First, we fitted a full model containing the random
factor ‘experimental agroforest’, and the terms of interest: (i)
three binary exclusion variables and their interaction terms, (ii)
agroforest-level design variables (canopy cover, forest distance)
and (iii) their interaction with each exclusion treatment variable,
(iv) seven covariates: crown volume, mean d.b.h., temperature,
precipitation, non-crop tree richness, branch perimeter and pod
groove depth. A second-order polynomial term was included for
canopy cover, to allow for nonlinearity (Tscharntke et al. 2011).
Continuous explanatory variables were z-transformed. We fitted
the model using maximum likelihood and Gaussian (marketable
Fig. 1. Study area in the Napu valley of
Central Sulawesi, Indonesia. Bottom: The
red area indicates Sulawesi. Top left:
Topography of Sulawesi and study area
(black square). Top right: Cycles show
experimental cacao agroforests, filling style
indicates canopy cover (empty <30%, half
=3050%, filled >50%), white labels
show rainfall in mm, green area indicates
rain forest, reddish areas indicate houses,
and bright areas indicate open land and
lines indicate streets.
©2016 The Authors. Journal of Applied Ecology ©2016 British Ecological Society, Journal of Applied Ecology
Shade-dependent predation effects on crop yield 3
yield, yield per fruit, number of harvested fruit, leaf area, leaf
damage), overdispersion-corrected Poisson (arthropod abun-
dances), or binomial (proportions of infested fruits) distribution.
For Gaussian models, root- or log-transformed response variables
were used to meet assumptions of homoscedasticity and (approxi-
mate) normality of the residuals. Models were assessed with vari-
ance inflation factors and diagnostic plots for residual normality,
heteroscedasticity and leverage.
Secondly, retaining all variables of interest, the model was sim-
plified by keeping those covariates that contributed to the model,
as indicated by a multi-model inference procedure (‘MuMIn’ R-
package, AIC based). The tree crown volume differed between
treatments and negatively correlated with canopy cover
(F=2092, P=004). Therefore, we included crown volume as
a permanent covariate during all statistical analyses. Thirdly, the
same procedure was used to identify non-significant interactions
that were removed for model simplification and refitted a model
using restricted maximum likelihood. In the results section, vari-
ables of interest and their interactions were reported when rela-
tive variable importance values (proportion of models including
the variable vs. models excluding the variable out of the best set
of models, identified by delta AIC <2) exceeded 09 for main
effect interactions and 07 for covariates. We used the lme4 pack-
age in R (Bates et al. 2014; R Core Team 2014) and reported sta-
tistical significance from the final model using ANOVA Type II,
Wald chi-square test (Kuznetsova, Brockhoff & Christensen
2014).
To determine the mechanisms leading to differences in mar-
ketable yields, only predictors identified as important for mar-
ketable yield (see Appendix S13) were used on the following
responses: (i) open flowers, (ii) aborted small fruits and (iii) leaf
herbivory. To test patterns of herbivorous arthropod abundances,
incidence of pests and disease symptoms, and beneficial arthro-
pod abundances, we used: (i) fruit infestation of H. sulawesi and
C. cramerella, (ii) Sternorrhyncha, (iii) caterpillars >10 mm, (iv)
Coleoptera >10 mm, (v) Auchenorrhyncha, (vi) Dermaptera, (vii)
Neuroptera larvae, (viii) hunting spiders <4 mm, (ix) hunting spi-
ders 410 mm, (x) web spiders <4 mm, (xi) web spiders 4
10 mm, (xii) ants and (xiii) Diptera <4 mm.
Finally, changes in community composition were tested using
species richness, diversity, evenness and composition of ants and
birds along the gradients of canopy cover and forest distance.
The measurements were rarefied to 737 individuals per site for
ants and 122 individuals per site for birds. We conducted a
redundancy analysis and visualized community composition using
Minimum Convex Polygons (MCP) at the level of the agroforest
(birds) and experimental treatment (ants) and, finally, tested for
the influences of canopy cover, forest distance and treatment
using a permutation test (n=999). Separate analyses were con-
ducted for each variable, with both remaining variables and
crown volume being set as conditions. Crown volume and treat-
ment were not included for bird community analyses, as birds
were recorded at the agroforest level.
Results
EFFECTS OF PREDATOR EXCLUSION, CANOPY COVER
AND DISTANCE TO FOREST ON CACAO YIELD
Yields of control trees varied between 75% and 135% of
the average productivity per hectare of 540 kg ha
1
year
1
for Indonesia in 2012 (Fig. 2, Appendix S13.1; yield
Indonesia 2012: http://faostat3.fao.org). In control trees,
marketable yield, proportion of fruits without pest infesta-
tion and the number of harvested fruits peaked under 30
40% shade-tree canopy cover (Figs 2 and 3gl,
Appendix S13.1S13.3). Yield was affected by ant and bird
exclusion with magnitude and direction of effects
depending on shade-tree canopy cover. Yield was not
affected by bat exclusion (Fig. 2, Appendix S13.1).
Interactions between exclusion treatments were not
significant. Independently of predator exclusions,
marketable yields and numbers of harvested
fruits decreased with increasing forest distance (Appendix
S13.1S13.3).
ANT EXCLUSION
Ant exclusions reduced ant abundances by 6090%
(Fig. 5a; Appendix S13.11). Marketable yield, the number
of harvested fruit and fruit weight were reduced under ant
exclusion (Figs 2 and 3j,m; Appendix S13.1S13.3). Ant
abundances were positively correlated with marketable
yields while controlling for exclusion treatments (v
2
=722,
P<001).
Fig. 2. Effects of predator exclusion on
marketable cacao bean yield. Dry yield (y-
axis) of exclusion treatments (control =
continuous black, no ants =blue, no birds
=dotted red, no bats =dashed green)
dependent on percentage of canopy cover
(x-axis), grey line marks the average cacao
production of Indonesia 2012 (http://
faostat3.fao.org), and yield was standard-
ized to 12 months for plotting only.
v2
Intercept indicates influences of predator
exclusions, while v2
Slope indicates canopy
cover dependency of predator exclusions.
©2016 The Authors. Journal of Applied Ecology ©2016 British Ecological Society, Journal of Applied Ecology
4P. Gras et al.
Below 30% canopy cover, ant exclusions were associ-
ated with fewer flowers, and a trend towards fewer
aborted small fruits compared to control treatments
(Figs 3a,d; Appendix S13.4 and S13.5). Ant exclusion did
not affect pest and disease incidence at fruits (Fig. 3g;
Appendix S13.6). Canopy cover above 50% reversed the
(a) (b) (c)
(c) (d) (e)
(f) (g) (h)
(i) (j) (k)
(l) (m) (n)
Fig. 3. Effects of predator exclusion on cacao tree phenology. Small figures show the response of cacao trees to ant (left), bird (mid) or
bat (right) exclusion related to canopy cover (x-axis), each circle/dot corresponds to two trees, line types: control =continuous black, no
ants =blue, no birds =dotted red, no bats =dashed green. v2
Intercept indicates influences of predator exclusions, while v2
Slope indicates
canopy cover dependency of predator exclusions.
©2016 The Authors. Journal of Applied Ecology ©2016 British Ecological Society, Journal of Applied Ecology
Shade-dependent predation effects on crop yield 5
differences in aborted small fruits, with higher numbers in
ant exclusions than in controls (Fig. 3d). Losses of flowers
and small fruits were reflected in reduced numbers of har-
vested fruits under ant exclusion (Fig. 3j;
Appendix S13.3). Additionally, fruit weight was reduced
in the absence of ants (Fig. 3m; Appendix S13.2).
Abundances of lepidopteran caterpillars (>10 mm) and
beetles significantly increased in response to ant exclusions
while abundances of caterpillars (04 mm) and leafhoppers
remained unaffected (Figs 4aj; Appendix S13.7S13.10).
Leaf damage was increased in ant exclusions below 30%
canopy cover (v
2
=654, P=001; Appendix S13.16).
Spiders were largely unaffected by ant exclusion, with
only a trend towards small web-building spiders being
more frequent in ant exclusions below 30% canopy cover.
(Fig. 5d,g; Appendix S13.12 and S13.13). Below 30%
canopy cover, earwigs were absent, but when present,
their abundance was reduced in ant exclusions (Fig. 5j;
Appendix S13.14). Small beetles were more abundant
under ant exclusion and with above 50% canopy cover
(Fig. 5m; Appendix S13.15).
BIRD EXCLUSION
Compared to controls, marketable cacao yields were
slightly reduced in bird exclusions when canopy cover was
above 50%. Canopy cover below 30% lead to higher
yields in bird exclusions (500 kg ha
1
year
1
to
830 kg ha
1
year
1
, Fig. 2; Appendix S13.1). Comparable
patterns were found for flowers, aborted small fruits,
fruits without damage by pests such as H. sulawesi and C.
cramerella, and harvested fruits (Figs 3bh;
Appendix S13.4S13.7). Amounts of non-infected and
harvested fruits were significantly correlated (v
2
=3287,
P<001). The fruit weight remained unaffected by bird
exclusion (Fig. 3n; Appendix S13.3).
Caterpillar and beetle abundances remained unaffected
by bird exclusion, but abundances of Auchenorrhyncha
were reduced (Figs. 4bk, Appendix S13.7S13.10). Simul-
taneously, web-building spider abundance increased,
although this effect was only significant for large individu-
als (410 mm), where it was stronger over 50% canopy
cover (Fig. 5h, Appendix S13.13). Increases in small web
spiders (<4 mm) were marginally significant and tended to
be higher with canopy cover <30% (Fig. 5e,
Appendix S13.12). Small beetles (<4 mm) tended to be less
abundant with more than 30% canopy cover (Fig. 5n,
Appendix S13.15). Earwigs had lower densities due to bird
exclusion, an effect restricted to canopy cover higher than
40% (Fig. 5k, Appendix S13.14). Ants were not signifi-
cantly affected by bird exclusion (Fig. 5b,
Appendix S13.11). Yield effects of bird exclusion persisted
when adding ant abundance as a model covariate. Small
dipterans were less frequent under bird exclusions
(v2
Bird exclusion =659, P=001; Appendix S15.17 in Support-
ing Information).
BAT EXCLUSION
Excluding bats had no significant effect on marketable
yield. No effect could be detected on flowers, aborted
small fruits, fruit infestation by pests and diseases,
harvested fruits or fruit weight (Figs 2 and 3co;
Appendix S15.1S15.6). Bat exclusion was associated with
higher numbers of leaf hoppers and, for canopy cover
over 50%, higher numbers of large caterpillars (410 mm)
(Fig. 4f,l, Appendix S15.7/10). Small caterpillars or bee-
tles remained unaffected (Fig. 4a,i, Appendix S15.7/9).
Bat exclusion did not affect mesopredators smaller
than 4 mm in body length, but was associated with higher
spider and earwig abundance (Fig. 5co, Appendix
S15.1115).
ANT AND BIRD DIVERSITY ALONG THE CANOPY COVER
AND FOREST DISTANCE GRADIENT
Ant species composition (redundancy analysis, Fig. S14)
was similar across those treatments where ants were present
(F=076, P=084), but ant species composition strongly
changed with percentage of canopy cover (F=281,
P=0001) and forest distance (F =293, P=0001).
Species composition of the local bird assemblage
(redundancy analysis, Fig. S15) changed due to forest dis-
tance (F =131, P=003), but did not respond to canopy
cover (F =112, P=033). Shannon index, species
evenness and rarefied species richness of ants and birds
were independent of canopy cover and forest distance
(Fig. S16).
Discussion
Access by predators, percentage of shade-tree canopy
cover and distance to forest margin had economically rel-
evant impacts on cacao yield. While the negative effect of
forest distance was independent of predator exclusion,
percentage of canopy cover affected the impact of preda-
tors. Yield peaked at 3040% canopy cover. Canopy
cover below 15% or above 55% resulted in less than half
of the optimum yield. Ant exclusion reduced yields at
15% canopy cover from 600 to 300 kg ha
1
year
1
. Bird
exclusion decreased yields at 60% canopy cover from 400
to 250 kg ha
1
year
1
. Unexpectedly, bird exclusion
increased yields at 15% canopy cover from 600 to 900 kg
ha
1
year
1
. Bats had no effect on yield.
Canopy cover-dependent effects of ant and bird
exclusions in agroforests have never been shown previ-
ously, despite several recent studies targeting these
groups in tropical agroforestry (Wielgoss et al. 2014;
Maas et al. 2015b). Our results can partly be explained
by patterns in yield formation, as well as impacts on
herbivorous and predatory arthropods that were quanti-
fied by fogging the experimental trees at the end of the
study period.
©2016 The Authors. Journal of Applied Ecology ©2016 British Ecological Society, Journal of Applied Ecology
6P. Gras et al.
CANOPY COVER-DEPENDENT EFFECTS OF ANTS
Ants affect plants by tending/defending or predating/dis-
placing herbivores, but also predating/displacing predators
(such as spiders) and pollinators, spreading propagules of
plant pathogens (Wielgoss et al. 2014), pollinating flowers,
predating/dispersing seeds and changing soil conditions
(Bartlett 1961; Way 1963; Mestre et al. 2013b; 2014).
Their ecological dominance in tropical agroforestry sys-
tems likely affects trees in multiple ways (e.g. plant
growth, leaf and fruit development). In our study, impacts
of ant exclusion have their likely cause in the interaction
of arboreal ants and other arboreal organisms such as
herbivores: ants were excluded from trees and not the
ground below, tent-building species able to spread patho-
gens were absent, and ants are not able to pollinate cacao
(Leston 1970). Interference between ants and spiders has
been reported from tree crops (Pi~
nol, Espadaler & Ca~
nel-
las 2012; Mestre et al. 2012; Mestre, Bucher & Entling
2014 but see Mar
ın & Perfecto 2013). Here, and in con-
trast to what was observed in response to bird exclusion,
no significant change in spider abundance occurred under
ant exclusion, suggesting that ants do not limit the abun-
dance of spiders. Instead, ants reduced abundances of her-
bivores such as caterpillars and beetles that damage not
only leaves but also cacao flowers (YC personal observa-
(a) (b) (c)
(d) (e) (f)
(g) (h) (i)
(j) (k) (l)
Fig. 4. Effects of predator exclusion on cacao tree herbivores. Small figures show the response of herbivores to ant (left), bird (mid) or
bat (right) exclusion related to canopy cover (x-axis), each circle/dot corresponds to two trees, line types: control =continuous black, no
ants =blue, no birds =dotted red, no bats =dashed green, v2
Intercept indicates influences of predator exclusions, while v2
Slope indicates
canopy cover dependency of predator exclusions.
©2016 The Authors. Journal of Applied Ecology ©2016 British Ecological Society, Journal of Applied Ecology
Shade-dependent predation effects on crop yield 7
tion; Bos, Steffan-Dewenter & Tscharntke 2007a; Maas,
Clough & Tscharntke). Increased herbivore abundance,
parallel increased leaf damage and fewer flowers under
ant exclusion probability resulted in fewer fruits.
Simultaneously, reinforcing negative effects on yield, fruit
weight was reduced when ants were absent, which is asso-
ciated with infestation by fruit-damaging pests such as H.
sulawesi and C. cramerella (Wielgoss et al. 2014). Impacts
(a) (b) (c)
(d) (e) (f)
(g) (h) (i)
(j) (k) (l)
(m) (n) (o)
Fig. 5. Effects of predator exclusion on cacao tree mesopredators. Small figures show the response of mesopredators to ant (left), bird
(mid) or bat (right) exclusion related to canopy cover (x-axis), each circle/dot corresponds to two trees, line types: control =continuous
black, no ants =blue, no birds =dotted red, no bats =dashed green, v2
Intercept indicates influences of predator exclusions, while v2
Slope
indicates canopy cover dependency of predator exclusions.
©2016 The Authors. Journal of Applied Ecology ©2016 British Ecological Society, Journal of Applied Ecology
8P. Gras et al.
of ants on crop yield, including their economic impor-
tance, are similar to those reported from sites situated in
the same region at lower altitudes (Wielgoss et al. 2014),
but our results demonstrate that ant predation effects
were only economically relevant for agroforests providing
<40% canopy cover. Generally, low-shade conditions can
be more stressful for cacao trees, both in terms of eco-
physiology, and in terms of herbivory (De Almeida &
Valle 2007; Tscharntke et al. 2011). These findings are in
accordance with our results, showing that small beetles
and caterpillar densities increased under low-shade condi-
tions. Besides this, we could show that there was signifi-
cant ant species turnover across the gradient in canopy
cover. It thus cannot be excluded that ant species more
dominant under low-canopy cover conditions provide a
more effective pest control than species dominant under
high-canopy cover.
BIRD EXCLUSIONS CAN DECREASE OR INCREASE
YIELDS DEPENDING ON CANOPY COVER
Against expectation, excluding birds led to more fruits and
higher proportions of healthy fruit below 30% canopy
cover. Lowered or similar yields under bird exclusion would
have been expected throughout the canopy cover gradient,
but were observed only in relation to canopy cover above
40%. We assume that the effects of excluding birds are
caused by the absence of insectivorous birds, of which 31
species were recorded at cacao canopy level (Maas et al.
2015a). Indeed, none of the bird species recorded feed on
cacao fruits. Woodpecker damage can occasionally be seen
on fruit (YC personal observation), but is likely to only
affect fruit with prior pest infestation. Pollination reduction
due to bird exclusion is unlikely, since cacao flowers are very
small and pollinated by midges, not birds (Leston 1970).
The bird community composition did not change with
canopy cover, suggesting that shade dependency of yields
under bird exclusions may be due to observed differences in
arthropod pest and mesopredator densities along the gradi-
ent. Generally, there was little response in herbivore abun-
dance to bird exclusion. Leafhopper numbers were
depressed and earwig numbers promoted under bird exclu-
sion when canopy cover was below 30%. This, together with
lower numbers of damaged fruits under bird exclusion,
points to indirect positive effects on herbivores by birds
(e.g. mesopredator predation) under little-shaded condi-
tions where herbivory affects cacao trees more severely
(Tscharntke et al. 2011). The exact mechanism is unclear, as
the fogging data show only a trend towards increases in
predator densities at canopy cover below 30% for ants and
small web spiders with increases and decreases at canopy
cover above 50% for larger web spiders and earwigs, respec-
tively. Generally, increased abundances of predators, such
as ants, spiders and earwigs, under bird exclusions, are com-
mon (Gunnarsson 2007; Williams-Guill
en, Perfecto & Van-
dermeer 2008; Pi~
nol et al. 2010; Maas, Clough &
Tscharntke 2013; Mestre et al. 2013a). Overall, increases in
most predatory arthropods and decreases in individual her-
bivores due to bird exclusion suggest mesopredator release
and may at least partly explain the ambivalent effects of
birds on cacao yield in our study, although food web data
will be necessary to confirm this. The impact of lower abun-
dances in small Dipterans (<4 mm), which includes cacao-
pollinating Ceratopogonidae (Leston 1970), is unknown,
yet could conceivably reduce pollination and thereby cause
yield losses (Groeneveld et al. 2010).
BATS
In 2010, at least 16 insectivorous bat species were
recorded in agricultural areas around the Lore Lindu
National Park in two separate studies by Graf and Boon-
man (unpublished data, Table S17). Several of the species
glean insects from leaves or perch on plants to prey on
arthropods associated with plants and might therefore be
relevant to our experimental exclusions. However, bat
exclusion did not affect yield, or yield-related plant vari-
ables, but enhanced abundances of leafhoppers, large
caterpillars, and earwigs and large spiders, that is both
herbivorous and predatory arthropods. Bats have strong
effects on arthropod communities in tropical forests and
agricultural systems (Kalka, Smith & Kalko 2008; Wil-
liams-Guill
en, Perfecto & Vandermeer 2008; Wanger et al.
2014). In coffee, bats can promote herbivorous arthro-
pods by reducing spider densities and, as a result, do not
necessarily provide biocontrol (Karp & Daily 2014). A
previous study from cacao in our study region, however,
showed bats were instrumental in decreasing pests (Maas,
Clough & Tscharntke 2013). This suggests that impacts of
bats could be strongly dependent on the net balance of
arthropod herbivores and predators, with bat impacts on
both groups cancelling out any top-down effect on the
plants in the present study. Leaf-gleaning bats are less
abundant in agricultural systems than in natural forest
(Phommexay et al. 2011) suggesting natural forests are
sources of bats for nearby agroforests, but we did not find
any evidence for forest distance-dependent effects of bats.
STUDY LIMITATIONS AND CAVEATS
The extent to which we can causally underpin the detected
significant effects is limited by the study design in some
respects. First, the impact of forest distance on yield, while
significant, cannot be fully elucidated, as it seems not to
involve the manipulated predators. Secondly, while we tried
to control for variables that could not be standardized,
unwanted exclusion effects may have occurred. For
instance, reduced earwig abundances under ant exclusion
may have been due to the ant exclusion rings partly exclud-
ing crawling earwigs. While this may have led to overesti-
mated impacts of ants under high-canopy cover, impacts of
ants were strongest below 30% canopy cover, where ear-
wigs were scarce, so our conclusions on ant effects are
robust. Moreover, earwig abundances that increased over
©2016 The Authors. Journal of Applied Ecology ©2016 British Ecological Society, Journal of Applied Ecology
Shade-dependent predation effects on crop yield 9
40% canopy cover in bat exclusions did not affect cacao
yield. Thirdly, we cannot exclude that the presence of nets
deterred certain birds or bats from foraging inside the agro-
forests, due to the risk of collision. Finally, the drawback of
a long study duration was the impossibility of adequately
surveying arthropods during the whole course of the experi-
ment. Parallels between herbivores and predators recorded
through fogging, and cacao tree variables recorded over the
whole study duration, allow us to draw hypotheses on
mechanisms, but not to formally test them.
MANAGEMENT RECOMMENDATIONS
Impacts of ants and birds on cacao yield are economically
relevant, but depend on shade-tree management. In all but
most shaded agroforests, ants were pivotal in supporting
yields, reducing populations of herbivorous insects rather
than other beneficial organisms such as spiders. This con-
firms the importance of ants for the economic performance
of cacao agroforestry in Central Sulawesi. Farmers should
be aware of changes in ant communities due to shifts in
management or species invasion, and avoid destroying ant
nests, as commonly done for weaver ants, for example
(YC & PG personal observation). Moreover, current cacao
farming methods entail self-shaded or low-shaded (~10%
shade-tree canopy cover) plantations impairing arthropod
and plant diversity (Rice & Greenberg 2000). The observa-
tion that, on average, shade-tree canopy cover of 3040%
yielded most, suggests that farmers should maintain such
intermediate canopy cover levels not only for ecophysio-
logical reasons (Tscharntke et al. 2011), but also to buffer
variability in predator communities. Our data suggests
that beneficial effects of forest proximity on yield were
unlikely to be related to pest limitation services by ants
and birds. However, positive effects of forest proximity on
predation of dummy caterpillars, mediated by higher
abundances of a locally common white-eye species Zos-
terops chloris, have been demonstrated in our study area
(Maas et al. 2015a), and together these results suggest that
farmers should have an interest in the stability of forest
margins, which are threatened by encroachment.
Acknowledgements
We are grateful to partners at Tadulako University, IPB and LIPI. We
thank Arjan Boonman and Stefan Graf for providing bat survey data of
our study region, Akhmad Rizali (ants), Hardianto Mangopo (trees) and
Firdaus (herbs) for specimen identifications and Arno Wielgoss, Iris
Motzke, Ilfianty Kasmundin and Pak Abdul Rauf for support. Special
thanks we address to all research (Dadang Dwi-Putra, Edi Djismin, Alfi-
anus Rumede), laboratory (Ivon, Abe and Fatma) and field assistants
(Opu, Nimus, Anto, Tia, Papa Ifer, Idi, Soni, Wandi, Anki, Sardin and
Sony), all farmers and project members, especially Wolfram Lorenz. The
project was funded by DFG (ELUC CL-474/1-1 and CRC 990 EFForTS).
Data accessibility
Data are available through EFForTS-Information System
(https://efforts-is.uni-goettingen.de) and Dryad Digital Repository
doi: 10.5061/dryad.90329 (Gras et al. 2016).
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Supporting Information
Additional Supporting Information may be found in the online version
of this article.
Fig. S1. Schematic experimental design.
Table S2. Non-crop tree species within chemical application free
area.
Table S3. Herbal plant species.
Table S4. Discovered ant species.
Table S5. Discovered bird species.
Table S6. Ant and bird community.
Fig S7. Open bat exclusion.
Fig. S8. Conical-shaped ant exclusion rings (without insect glue).
Table S9. Potentially yield influencing variables (additional to the
predator exclusion).
Table S10. Characteristics of experimental trees and plantations at
treatment level.
Table S11. Fruit development categories.
Table S12. Pest and disease categories.
Appendix S13. ANOVA Tables.
Fig. S14. RDA Management, landscape, and predator access
manipulation influences on the ant community composition (mor-
pho species level).
Fig. S15. RDA Management and landscape effects on the bird
community (species level).
Fig. S16. Visualization of bird and ant community composition
related to shade cover and forest distance.
Table S17. Bat species.
©2016 The Authors. Journal of Applied Ecology ©2016 British Ecological Society, Journal of Applied Ecology
Shade-dependent predation effects on crop yield 11
... To measure tree productivity and pod damage, we counted all cacao flowers and fruits, as well as presence/absence of pest and disease symptoms on each pod. Following Gras et al. (2016), we classified fruits into small (0-9 cm), large (> 9 cm) and ripe categories according with their sizes and colour. We divided pod damage into six categories: Black Pod Disease, Capsid Pest Feeding, Dead Black Tissue, Cherelle Wilt, Immature Ripening, and vertebrate feeding (see Section 2 in Appendix for more details). ...
... Cacao production usually decreases with increasing plantation-level shade cover, with studies pointing to a maximum of 30-40 % shade to maintain partial win-win scenarios for farmers and biodiversity Clough et al., 2011;Gras et al., 2016). In our study, we recorded a constant decrease in the number of large pods with increasing tree-level shade cover in exclosures but an increase when bats and birds were present (Fig. 4B). ...
... In our study, we recorded a constant decrease in the number of large pods with increasing tree-level shade cover in exclosures but an increase when bats and birds were present (Fig. 4B). Although we could not find a direct link between pod damage and cacao yield, bats and birds are known to increase productivity through pest suppression in different agroforestry systems , with these services being higher in plantations with high plantation-level shade cover and forest proximity (Gras et al., 2016;Librán-Embid et al., 2017). However, none of pest groups studied here increased in numbers with increasing tree-level shade cover and even the Hemipteran insects showed the opposite pattern, decreasing in exclosures and increasing in controls with increasing tree-level shade cover (Fig. 4B). ...
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Central/West Africa is one of the most biodiverse regions on earth and one of the largest producers of cacao, producing about 68.4 % of the world's chocolate. Here, cacao pests and diseases can cause losses of $761 million annually. However, no studies from Africa have quantified the role of flying vertebrates as pest suppressors in cacao plantations. We used an exclusion experiment to prevent access of bats and birds to cacao trees for 12 months and quantified how their absence affected arthropod communities, herbivory, and cacao crop yield. Overall, important pests such as mealybugs and other hemipterans were more abundant in exclosures (9 and 1.6 times increase, respectively), despite potential multitrophic interactions with simultaneously increasing predatory arthropods such as spiders and mantis. Under heavy shade (90 %), cacao trees with flying vertebrate exclosures had 3.9 times fewer flowers and 3.2 times fewer large pods than control trees, corresponding to estimated losses on average of $478 ha⁻¹y⁻¹. Under low tree-level shade cover (10 %) however, the opposite pattern was evident: exclosure trees had 5.2 times more flowers and 3.7 times more large pods than control trees, corresponding to estimated savings on average of $796 ha⁻¹y⁻¹. We demonstrate that the enormous potential of African flying vertebrates as pest suppressors in cacao plantations is dependent on local shade tree management and only economically relevant above 50 % of shade. Despite higher productivity at low shade levels, our findings encourage African policymakers and farmers to adopt more high shade cacao agroforestry systems to maximize pest suppression services provided by bats and birds.
... These nature-based services are biodiversity-driven [3] and provided by multiple animal groups. Vertebrates such as birds and bats, as well as arthropods, may control pest populations [4,5], while bees and many other animals are important crop pollinators [6]. But animals can also cause substantial disservices: some herbivorous arthropod species are pests threatening yields of many crops. ...
... Other vertebrates, such as squirrels and other rodents, prey on mature cacao fruits and can cause severe harvest losses [8]. Harvest loss can also be due to fungal infections, and by propagating fungal spores, ants can enhance fruit loss [5,10,18]. However, ants can also support yield gains, through reduction in flower and leaf herbivory [5]. ...
... Harvest loss can also be due to fungal infections, and by propagating fungal spores, ants can enhance fruit loss [5,10,18]. However, ants can also support yield gains, through reduction in flower and leaf herbivory [5]. Knowledge on combined effects of animal groups is critical to improving our understanding of services and disservices, which in turn might allow developing more efficient management recommendations for profitable and sustainable biodiversity-friendly cacao agroforestry. ...
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Animals provide services such as pollination and pest control in cacao agro-forestry systems, but also disservices. Yet, their combined contributions to crop yield and fruit loss are mostly unclear. In a full-factorial field experiment in northwestern Peru, we excluded flying insects, ants, birds and bats from cacao trees and assessed several productivity indicators. We quantified the contribution of each group to fruit set, fruit loss and marketable yield and evaluated how forest distance and canopy closure affected productivity. Fruit set dropped (from 1.7% to 0.3%) when flying insects were excluded and tripled at intermediate (40%) compared to high (greater than 80%) canopy cover in the non-exclusion treatment. Fruit set also dropped with bird and bat exclusion, potentially due to increased abundances of arthropods preying on pollinators or flower herbivores. Overall, cacao yields more than doubled when birds and bats had access to trees. Ants were generally associated with fruit loss, but also with yield increases in agroforests close to forest. We also evidenced disservices generated by squirrels , leading to significant fruit losses. Our findings show that several functional groups contribute to high cacao yield, while trade-offs between services and disservices need to be integrated in local and landscape-scale sustainable cacao agroforestry management.
... c'est un atout pour le contrôle biologique dans les paysages simplifiés et un désavantage dans les paysages complexes, car la prédation intraguilde perturbe la régulation des ravageurs de culture (Martin et al., 2013 ;Olimpi et al., 2020). Cependant, l'inverse a également été mis en avant (Gras et al., 2016). ...
... The unexpected increase in Araneae abundance when birds were present (i.e., control plot versus cage) suggested no intraguild predation conversely to previous studies (Bosc et al., 2018;Gras et al., 2016;Maas et al., 2013;Mestre et al., 2013). However, our results provided no reliable explanations for this positive relationship, which did not hold true in SEM models based on abundances. ...
Thesis
La dépendance de l'agriculture aux pesticides peine à se réduire et la biodiversité dans les milieux agricoles continue de décliner. Les systèmes de culture d’aujourd’hui doivent progresser vers un renforcement des processus écologiques pour tendre vers une gestion agroécologique de la santé des cultures, ce qui nécessite d’approfondir nos connaissances sur la régulation effectuée par les prédateurs et parasitoïdes, ainsi que leurs déterminants. Par ailleurs, très peu de connaissances établies en parcelles agricoles existent sur la multifonctionnalité de systèmes de grandes cultures.La thèse a pour objectifs d'évaluer (i) comment des bandes fleuries pérennes insérées dans des systèmes de culture contrastés, modifient les communautés multitrophiques, les régulations biologiques, et les biens et services écosystémiques qui peuvent en résulter, et (ii) la multifonctionnalité des systèmes de culture adossés à une bande fleurie. À cette fin, un réseau de 31 agriculteurs qui mettent en place des systèmes de cultures en agriculture biologique, de conservation des sols (ACS) ou conventionnels, est mobilisé dans le bassin parisien. Au sein de ce réseau, nous avons comparé des couples de parcelles de grandes cultures avec et sans bande fleurie, et caractérisé la biodiversité, les services de régulation biologique sur plusieurs cultures, le service culturel et des performances agronomiques et économiques.Nos résultats montrent tout d’abord que l’effet des bandes fleuries dépend du type de système de culture dans lequel elles sont implantées et du taxon considéré. La régulation des bioagresseurs du colza est peu affectée par la présence d’une bande fleurie mais elle augmente avec les ressources trophiques fournies par les adventices dans les parcelles.Sur féverole, les ressources trophiques en bord de champ permettent d’augmenter les abondances de syrphes et de momies de pucerons verts, mais cela ne s’est pas traduit par une régulation accrue des pucerons. L’analyse du réseau trophique suggère que les oiseaux sont peu connectés aux arthropodes épigés et ne prédatent pas les prédateurs. Nos résultats indiquent aussi un rôle important des carabes dans les régulations biologiques d’insectes phytophages.Dans un second temps, une enquête auprès des citoyens sur la perception esthétique et de la biodiversité de parcelles agricoles nous a révélé une préférence marquée pour les systèmes de culture dont le sol est le plus couvert et dont la végétation, cultivée ou non, est diversifiée. Ces systèmes s’apparentent à ceux en ACS.Enfin, nous avons évalué la multifonctionnalité des systèmes de culture, dans des parcelles avec ou sans bandes fleurie. Les systèmes de culture ayant fortement recours à la biodiversité montrent un profil plus équilibré entre les biens et services fournis. Les systèmes de culture en ACS ou très diversifiés sont un peu moins performants sur le plan agronomique et économique mais sont plus performants sur le service culturel, et semblent plus favorables à la biodiversité lorsqu’ils sont associés à une bande fleurie.En conclusion, nous montrons une complémentarité entre la présence d’une bande fleurie et les différents systèmes de culture dans la fourniture de biens et services écosystémiques. Ils suggèrent que les systèmes basés sur la biodiversité, dans la parcelle et ses abords, renforcent le profil de multifonctionnalité des systèmes de culture.
... They also reported a non-significant difference in final yield between the experimental and control plots. Similar non-significant differences in final yield have also been reported from other crops like cacao (Gras et al., 2016), and coffee (Karp and Daily, 2014). ...
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Insectivorous bats are gaining increasing attention for their potential as biological agents of pest suppression. Studies around the world have demonstrated their tendency to track and hunt agricultural pests over time and space, and thus to have a positive impact on reducing plant damage and protecting yield of agricultural crops. We documented the effect of insectivorous bats on the health and yield of a rice crop in Assam, India. Using six sets of paired experimental and control plots (of which five were analysed), where bats were selectively excluded from the experimental plots, we collected two measures of plant damage and one measure of total yield to assess the impact of bats on the crop. In parallel, bat activity at the six sites was recorded over the rice growing season using passive acoustic recorders. Our results show that the exclusion of insectivorous bats causes an increase in the degree of defoliation suffered by rice plants. We also report non-significant differences in the degree of yellowing of rice and of the total yield between the experimental and control plots. Bat activity levels showed a mono- or bi-modal peak in activity over the growing season, which broadly tracked the maturity of rice, a pattern also seen in many insect pests. Our results strongly suggest that bats have suppressive impact on pest action in rice fields. The general trend in activity levels, as well as the significant difference in plant damage, would indicate that bats are hunting insect pests and that the non-significant difference in final yield was likely the result of methodological limitations. These findings suggest that bats add significant ecological and economic value to Indian rice ecosystems and hold great potential to be used in integrated pest management (IPM) strategies aimed at suppressing pests.
... Such information is important, as it can contribute to our fundamental understanding of spatial variation in pest and pathogen dynamics on understory plants. From an applied perspective, the informed selection and planting of trees has the potential to reduce pest and disease levels, and might therefore contribute to an increase in crop yield in agroforestry systems and the conservation of rare understory plants in natural systems (Barrios et al., 2012;Durand-Bessart et al., 2020;Gras et al., 2016). ...
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The multifunctional role of shade trees for conservation of biodiversity and ecosystem services in natural forests and agroforests is well documented, yet we lack insights into the impact of shade tree species identity on pest and disease dynamics on agroforestry crops such as coffee and cacao, and its implications for management. We conducted two surveys on the impact of shade tree species identity and canopy cover on pests, diseases and a fungal hyperparasite on Arabica coffee in southwestern Ethiopia, which is one of the areas of origin of Arabica coffee. One survey was in a commercial plantation, and the other along a management gradient from only little managed coffee growing in the natural forest to intensively managed commercial plantations. To link these findings to current shade tree selection criteria, we complemented these surveys by interviews with farmers and managers. Shade tree species identity left a weak imprint on insect pest levels, and insect pests levels differed strongly in the strength and direction of their response to canopy cover. In contrast to the insect pests, the incidence of coffee leaf rust and its hyperparasite, as well as coffee berry disease, differed among shade tree species, with particularly high levels of coffee leaf rust and the hyperparasite underneath the canopy of the shade trees Acacia abyssinica and Croton macrostachyus, and coffee berry disease underneath the canopy of Acacia abyssinica and Polyscias fulva. Smallholder farmers used many criteria for selecting shade trees, such as leaf traits and competition for soil moisture, but low priority is given to the effect of shade tree species identity on pests and diseases. Our findings help to understand spatial variation in pest and disease dynamics in natural forests and agroforests, and may inform the selection of shade tree species by coffee producers and thereby contribute to ecologically-informed pest and disease management. Importantly, our finding highlight the potential for using tree identity for the sustainable management of pests and diseases, with relevance for global agroforestry systems.
... Epiphytic plants such as bromeliads have been shown to act as keystone species for the maintenance of ant communities and services [47]. Their architectural morphometry and the suspended soil formations associated with their roots are pivotal in structuring the forest canopy, providing vital nesting microhabitats, and offering foraging opportunities for a range of ant species [48]. ...
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Ants often interact with other invertebrates as predators or mutualists. Epiphytic bromeliads provide nesting sites for ants, and could increase ant abundances in the tree canopy. We surveyed ants in the foliage of orange trees that either hosted bromeliads or did not. To determine if observed associations between bromeliads and tree ants were causal, we removed bromeliads from half of the trees, and resurveyed ants six weeks later. Our results show that bromeliad presence is correlated with higher ant abundances and different species of ants on orange trees during the dry season. This increase in ant abundance was driven primarily by Solenopsis ants, which were both numerous and found to facultatively nest in bromeliads. Bromeliad removal did not affect either ant abundance or composition, potentially because this manipulation coincided with the transition from dry to wet season. Other ant species were never encountered nesting in bromeliads, and the abundances of such ants on tree leaves were unaffected by bromeliad presence or removal. Considering the importance of ants in herbivore regulation, our findings suggest that bromeliads-through their association with ants-could indirectly be associated with biological control in agricultural systems.
... Exclusion studies show a direct relationship between the absence of bats and increase in crop pests, as evidenced by Maine and Boyles (2015), who found that excluding bats from their study site led to 59% more corn earworm larvae/ear (Kalka et al., 2008;Maas et al., 2013). For example, exclosure of birds and bats resulted in increased arthropod herbivory in Indonesian cacao agroforestry systems (Maas et al., 2013;Gras et al., 2016). In contrast, the absence of bats resulted in increased crop damage by 56% as compared to controls and increased larval density of the corn ear moth in maize fields in Illinois (Maine and Boyles, 2015). ...
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The fall armyworm (FAW, Spodoptera frugiperda) is a major crop pest in southern Africa. It threatens the livelihoods and food security of smallholder farmers in the region by negatively impacting maize yield. Although scientific evidence suggests that natural enemy-mediated predation can potentially reduce FAW infestation, the effectiveness of natural enemies such as birds, bats, parasitoids, and generalist predators on FAW is poorly understood. This study reviews existing literature to assess how birds, bats, parasitoids, and generalist predators’ control FAW infestation, as well as the role of forest or tree cover in natural enemy mediated pest control of FAW in maize in southern Africa. We then present a case study to examine the role of forest proximity in reducing FAW infestation in maize in Zimbabwe. We conclude that birds, bats, parasitoids, and generalist predators are likely drivers of the reduced success of FAW near forests in southern Africa. While predators influence FAW survival and development, their role is largely undermined by parasitoids, which are more efficient in affecting FAW populations. Birds, bats, parasitoids, and generalist predators play an important role in controlling FAW on farms in heterogenous landscapes with diverse vegetation and near-forest proximity. The findings of our case study from Zimbabwe suggest that the distance to forest had a much higher impact on FAW incidence than maize variety, planting date, or the rate of nitrogen applied. Lack of enough case studies from maize in southern Africa makes it challenging to assess the mechanism and the effectiveness of bird predation on FAW. For this reason, further research is necessary to examine how predation by birds, bats and arthropods and parasitism impacts maize yield. We discuss research barriers, recommend appropriate methods for experimental studies, and suggest possible management options to control FAW in southern Africa.
... The value of ants for pest-control has long been recognized as ants are voracious predators of plant herbivores and can reduce herbivory (Hölldobler & Wilson, 1990), but only more recently have studies partitioned out the value of ants versus other taxa; for example, Piñol et al. (2010) demonstrated that ants had a greater effect regulating arthropod populations on citrus than birds did. The predation biocontrol service provided by ants is especially valued in agricultural systems with studies suggesting ants can significantly promote crop yields (e.g., in shade cocoa, Gras et al., 2016). In addition, ant pest-control services extend to weed control too: in an Australian agricultural system, the presence of ants reduced the number of tumbleweed plants by almost a half (Evans & Gleeson, 2016). ...
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Ants (Hymenoptera: Formicidae) are one of the most dominant terrestrial organisms worldwide. They are hugely abundant, both in terms of sheer numbers and biomass, on every continent except Antarctica and are deeply embedded within a diversity of ecological networks and processes. Ants are also eusocial and colonial organisms-their lifecycle is built on the labor of sterile worker ants who support a small number of reproductive individuals. Given the climatic changes that our planet faces, we need to understand how various important taxonomic groups will respond; this includes the ants. In this review, we synthesize the available literature to tackle this question. The answer is complicated. The ant literature has focused on temperature, and we broadly understand the ways in which thermal changes may affect ant colonies, populations, and communities. In general, we expect that species living in the Tropics, and in thermally variable microhabitats, such as the canopy and leaf litter environments, will be negatively impacted by rising temperatures. Species living in the temperate zones and those able to thermally buffer their nests in the soil or behaviorally avoid higher temperatures, however, are likely to be unaffected or may even benefit from a changed climate. How ants will respond to changes to other abiotic drivers associated with climate change is largely unknown, as is the detail on how altered ant populations and communities will ramify through their wider ecological networks. We discuss how eusociality may allow ants to adapt to, or tolerate, climate change in ways that solitary organisms cannot and we identify key geographic and phylogenetic hotspots of climate vulnerability and resistance. We finish by emphasizing the key research questions that we need to address moving forward so that we may fully appreciate how this critical insect group will respond to the ongoing climate crisis.
Thesis
The Northern Ecuadorian Amazon (NEA) is recognized as biodiversity hotspot that contains unique endemic plant species. However, unsustainable agricultural practices, such as more frequent cycles of shifting agriculture (SA), threat the NEA's forests endurance with negative consequences for biodiversity levels and ecological functions. In this study, I examined the spatial and temporal dynamics of the diversity of native trees across various types of agroforestry systems (AFS) subjected to SA. That is, the degree of existing risk of endangerment of tree species, the rapid change in floristic composition of mature forests converted to AFS, and the recovery pace of forest communities following abandonment. Transforming mature forest communities (MFC) to different AFS leads to a decrease in alpha diversity up to 75%. AFSs preserve 56% of the beta diversity compared to MFC; at least 8% of the species are threatened and the demographic status of 92% species is unknown. MFCs seem to regain their original structure after AFS abandonment. In the second part, I investigated whether AFS reverses the effect of intensified SA in cocoa (Theobroma cacao) agrosystems. I addressed the extent to which multispecific cocoa AFSs buffer the impact of reduced fallows in SA on loss of species. Tree diversity showed a gradual decrease from low to intermediate to high intensification SA in cocoa AFS, with values of 46, 29, and 12 species richness. The absence of fallows in SA affects tree presence, leading to changes in floristic composition in 30% fewer species compared to the beta diversity in cocoa AFSs experiencing long resting phases. Nonetheless, the similar beta diversity between low and intermediate intensification levels of SA suggests a concomitant delay in forest degradation rates. Finally, I examined the extent to which beta diversity in AFS reverses the effect of shorter SA fallow periods in the soil properties of cocoa (T. cacao) agrosystems. Agroforestry systems, combined with SA, shields the negative outcome of intense land-use on the soil's nutrients. The arboreal cover maintains the soil fertility needed for crop performance and food sustainability. The dominance of certain tree species (Vochysia leguiana, Inga edulis, Cordia alliodora) is essential to support adequate dynamic levels of nutrient cycling with more intense fallow periods, whereas some other species (Virola flexuosa, Chrysophyllum amazonicum, Ocotea bofo) have an apparent effect on soil acidity. I conclude that AFS have the potential for enhancing sustainable forest management and preservation of endangered tree species.
Chapter
Ecosystems provide a number of free services, especially provisioning services, on which humans depend for survival. All food comes from ecosystems; often ecosystems manipulated for crop or timber production. Fresh water also is a product of ecosystems, along with numerous medical and industrial products. In addition, ecosystems provide cultural services, such as recreational, religious, and educational uses. Supporting and regulatory services include processes, such as pollination, decomposition, and biological control, that contribute to production and delivery of harvestable resources. Insects often have been vilified as threats to human health and food production but also are important sources of food, water, medical and industrial products, cultural values, and inspiration for technological advances. An important challenge for resource and pest management professionals is how to manage pests without threatening the sustainability of ecosystem services.
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One of the frequent questions by users of the mixed model function lmer of the lme4 package has been: How can I get p values for the F and t tests for objects returned by lmer? The lmerTest package extends the 'lmerMod' class of the lme4 package, by overloading the anova and summary functions by providing p values for tests for fixed effects. We have implemented the Satterthwaite's method for approximating degrees of freedom for the t and F tests. We have also implemented the construction of Type I - III ANOVA tables. Furthermore, one may also obtain the summary as well as the anova table using the Kenward-Roger approximation for denominator degrees of freedom (based on the KRmodcomp function from the pbkrtest package). Some other convenient mixed model analysis tools such as a step method, that performs backward elimination of nonsignificant effects - both random and fixed, calculation of population means and multiple comparison tests together with plot facilities are provided by the package as well.
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Description Fit linear and generalized linear mixed-effects models. The models and their components are represented using S4 classes and methods. The core computational algorithms are implemented using the 'Eigen' C++ library for numerical linear algebra and 'RcppEigen' ``glue''.
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T op-down limitation of herbivores is an im-portant ecosystem service that facilitates agricultural production (1). Several experi-ments in natural and managed ecosystems demon-strate the importance of avian predators in arthropod control (2). Although insectivorous bats are ex-pected to have major impacts on arthropods (3), few studies have quantified the effects of bats on standing crops of arthropods. Because all previ-ous exclosure-based studies of avian insectivory have left exclosures up during the night, it is possible that a proportion of predation attributed to birds may represent predation by foliage-gleaning bats. Here, we report an exclosure experiment conducted in a Mexican coffee agroforest, in which we directly measured the impact of pre-dation by foliage-gleaning birds and bats on ar-thropods found on coffee plants. We used exclosures made of agricultural net-ting erected around individual coffee plants in Finca Irlanda, an organic shade coffee plantation harboring abundant populations of ≥120 bird species and ≥45 bat species. We established 22 blocks of four treatments: birds-only excluded (exclosure netting in place only during the day), bats-only excluded (netting in place only during the night), both excluded (netting in place day and night), and control (no netting). We visually censused noncolonial arthropods (primarily insects, but also spiders, harvestmen, and mites) on all plants at the beginning of the experiments, every 2 weeks thereafter, and at the end of the experiment. We conducted the experiment for a 7-week period beginning January 2007 (dry season) and for an 8-week period beginning June 2007 (wet season). Exclusion of birds and bats resulted in sig-nificant increases in total arthropods on experi-mental plants, although a significant amount of variation was also explained by foliage biomass and initial arthropod density (table S1). On average, total arthropod densities on plants from which both predators were excluded were 46% higher than those observed on control plants. There was a clear seasonal effect with regard to bats: Although bats did not have significant ef-fects on arthropod densities in the dry season, their impacts were highly significant in the wet season, with an 84% increase in arthropod den-sity in bat-only exclosures, exceeding the effects of birds (Fig. 1). In neither season was there a significant interaction between bats and birds, indicating an additive effect. Regardless of sea-son, arthropod densities increased the most on plants from which both birds and bats were ex-cluded (Fig. 1). These seasonal and additive pat-terns held for various arthropod taxa (table S2), although only birds significantly reduced spiders. Although predator exclusions resulted in increased arthropod density, no significant differences were seen between treatments in the prevalence or the intensity of leaf damage. At our site, bats were as important as birds in regulating insect populations across the course of the year. We suspect that increased impacts of birds in the dry season may result from an influx of insectivorous overwintering migrants from North America (4). We have no data on the ab-solute density of bats versus birds; however, at our site the capture rates (and presumably abundance) and reproductive activity of bats increased during the wet season. Bats' relatively higher surface area may result in greater heat loss and concom-itantly higher energy requirements (5), and reproduction increases females' energetic needs; thus, increased bat abundance and reproduction in the wet season may result in an increased impact of bat predation on understory arthropods. Our results are consistent with arguments that functional diversity is central to the main-tenance of ecosystem services (6). In this case, the presence of these two vertebrate taxa main-tains a functional difference that enhances the efficacy of arthropod reduction. Previous exclo-sure studies have not differentiated between diurnal and nocturnal predators, attributing ob-served changes to birds. We suggest that these studies of the impacts of "bird" predation may have underestimated the importance of bats in limiting insects. Bat pop-ulations are declining worldwide (7), but mon-itoring programs and conservation plans for bats lag far behind those for birds. Declin-ing bat populations may compromise critical eco-system services, making an improved understanding of their conservation status vital.
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Maximum likelihood or restricted maximum likelihood (REML) estimates of the parameters in linear mixed-effects models can be determined using the lmer function in the lme4 package for R. As for most model-fitting functions in R, the model is described in an lmer call by a formula, in this case including both fixed- and random-effects terms. The formula and data together determine a numerical representation of the model from which the profiled deviance or the profiled REML criterion can be evaluated as a function of some of the model parameters. The appropriate criterion is optimized, using one of the constrained optimization functions in R, to provide the parameter estimates. We describe the structure of the model, the steps in evaluating the profiled deviance or REML criterion, and the structure of classes or types that represents such a model. Sufficient detail is included to allow specialization of these structures by users who wish to write functions to fit specialized linear mixed models, such as models incorporating pedigrees or smoothing splines, that are not easily expressible in the formula language used by lmer.
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Understanding distribution patterns and multitrophic interactions is critical for managing bat- and bird-mediated ecosystem services such as the suppression of pest and non-pest arthropods. Despite the ecological and economic importance of bats and birds in tropical forests, agroforestry systems, and agricultural systems mixed with natural forest, a systematic review of their impact is still missing. A growing number of bird and bat exclosure experiments has improved our knowledge allowing new conclusions regarding their roles in food webs and associated ecosystem services. Here, we review the distribution patterns of insectivorous birds and bats, their local and landscape drivers, and their effects on trophic cascades in tropical ecosystems. We report that for birds but not bats community composition and relative importance of functional groups changes conspicuously from forests to habitats including both agricultural areas and forests, here termed 'forest-agri' habitats, with reduced representation of insectivores in the latter. In contrast to previous theory regarding trophic cascade strength, we find that birds and bats reduce the density and biomass of arthropods in the tropics with effect sizes similar to those in temperate and boreal communities. The relative importance of birds versus bats in regulating pest abundances varies with season, geography and management. Birds and bats may even suppress tropical arthropod outbreaks, although positive effects on plant growth are not always reported. As both bats and birds are major agents of pest suppression, a better understanding of the local and landscape factors driving the variability of their impact is needed. © 2015 Cambridge Philosophical Society.
Article
Avian ecosystem services such as the suppression of pests are considered to be of high ecological and economic importance in a range of ecosystems, especially in tropical agroforestry. However, how bird predation success is related to the diversity and composition of the bird community, as well as local and landscape factors, is poorly understood.We quantified arthropod predation in relation to the identity and diversity of insectivorous birds using experimental exposure of artificial, caterpillar-like prey in 15 smallholder cacao agroforestry systems differing in local shade-tree management and distance to primary forest. The bird community was assessed using both mist-netting (targeting active understorey insectivores) and point counts (higher completeness of species inventories).Bird predation was not related to local shade-tree management or overall bird species diversity, but to the activity of insectivorous bird species and the proximity to primary forest. Insectivore activity was best predicted by mist-netting-based data, not by point counts. We identified the abundant Indonesian endemic lemon-bellied white-eye Zosterops chloris as the main driver of predation on artificial prey.Synthesis and applications. The suppression of arthropods is a major ecosystem service provided by insectivorous birds in agricultural systems world-wide, potentially reducing herbivore damage on plants and increasing yields. Our results show that avian predation success can be driven by single and abundant insectivorous species, rather than by overall bird species richness. Forest proximity was important for enhancing the density of this key species, but did also promote bird species richness. Hence, our findings are both of economical as well as ecological interest because the conservation of nearby forest remnants will likely benefit human needs and biodiversity conservation alike.
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The loss of apex predators is known to have reverberating consequences for ecosystems, but how changes in broader predator assemblages affect vital ecosystem functions and services is largely unknown. Predators and their prey form complex interaction networks, in which predators consume not only herbivores but also other predators. Resolving these interactions will be essential for predicting changes in many important ecosystem functions, such as the control of damaging crop pests. Here, we examine how birds, bats, and arthropods interact to determine herbivorous arthropod abundance and leaf damage in Costa Rican coffee plantations. In an exclosure experiment, we found that birds and bats reduced non-flying arthropod abundance by -35% and -25%, respectively. In contrast, birds and bats increased the abundance of flying arthropods, probably by consuming spiders. The frequency of this intraguild predation differed between birds and bats, with cascading consequences for coffee shrubs. Excluding birds caused a greater increase in herbivorous arthropod abundance than excluding bats, leading to increased coffee leaf damage. Excluding bats caused an increase in spiders and other predatory arthropods, increasing the ratio of predators to herbivores in the arthropod community. Bats, therefore, did not provide benefits to coffee plants. Leaf damage on coffee was low, and probably did not affect coffee yields. Bird-mediated control of herbivores, however, may aid coffee shrubs in the long-term by preventing pest outbreaks. Regardless, our results demonstrate how complex, cascading interactions between predators and herbivores may impact plants and people.