Mutualism with aphids affects the trophic position,
abundance of ants and herbivory along an elevational gradient
SHUANG ZHANG, YUXIN ZHANG,
AND
KEMING MA State Key Laboratory of Urban and Regional Ecology, Research Center for Eco-Environmental Sciences,
Chinese Academy of Sciences, Beijing 100085 P. R. China
Citation: Zhang, S., Y. Zhang, and K. Ma. 2015. Mutualism with aphids affects the trophic position, abundance of ants
and herbivory along an elevational gradient. Ecosphere 6(12):253. http://dx.doi.org/10.1890/ES15-00229.1
Abstract.Varied interspecific interactions have a tremendous impact on the population dynamics of
related species. However, the context dependency of interspecific interactions and their ecological effects
have not been well-characterized. To understand the context dependency of ant-aphid mutualism and the
corresponding ecological effects, we explored the association of ant abundance, trophic position, and plant
herbivory along an elevational gradient. We hypothesized that a higher abundance of ants would be
associated with a lower trophic position and lower plant herbivory level along the gradient. We detected a
large variation in ant abundance and herbivory along the elevational gradient. Consistent with our
prediction, a higher ant abundance was associated with a lower trophic position, and herbivory decreased
linearly with ant abundance. A tight positive relationship between the abundance of ants and aphids was
observed. These findings suggest that the context dependency of ant-aphid mutualism can be an important
factor affecting the pattern of ant abundance and plant herbivory across the elevational gradient. This
study highlights the significance of mutualistic interactions in shaping the pattern of certain key ecological
processes, such as herbivory, at a relatively larger spatial scale.
Key words:ant–plant interactions; context dependency; environmental gradient; plant defense; tri-trophic interactions.
Received 18 April 2015; revised 16 July 2015; accepted 27 July 2015; published 11 December 2015. Corresponding Editor:
T. Roulston.
Copyright: Ó 2015 Zhang et al. This is an open-access article distributed under the terms of the Creative Commons
Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the
original author and source are credited. http://creativecommons.org/licenses/by/3.0/
E-mail: [email protected]
INTRODUCTION
(Chamberlain et al. 2014).
The ant-hemipteran interaction is a common
mutualistic interaction in nature (Way 1963,
Stadler and Dixon 2005). In these interactions,
ants protect hemipterans against predators; in
return, hemipterans offer ants honeydew, which
is rich in carbohydrates, as food (Way 1963,
Stadler and Dixon 2005). Honeydew is an
important food source for ants. Recent studies
have found that the experimental addition of
carbohydrate foods can enhance the activity,
aggressiveness, population size, and dominance
of ants within a community (Grover et al. 2007,
Heil 2008, Gibb and Cunningham 2009, Ness et
al. 2009, Byk and Del-Claro 2011, Pringle et al.
Context dependency is a major theme in the
study of interspecific interactions (Chamberlain
et al. 2014). Varied interspecific interactions can
have a tremendous impact on the population
dynamics of related species (Maron et al. 2014).
To date, the context dependency of interspecific
interactions and their ecological effects have not
been well-characterized, especially along environmental gradients (Maron et al. 2014). Exploring how interspecific interactions and their
ecological effects vary along an environmental
gradient is important for gaining insight into a
community’s response to a changing world
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ZHANG ET AL.
2011, Wilder et al. 2011a). Ants are omnivorous
insects in the field, and their trophic position can
range from pure herbivores to pure predators
(Blüthgen et al. 2003, Rico-Gray and Oliveira
2007). Because honeydew is a plant-based food
source, the more dependent that ants are on
honeydew, the lower their trophic position will
be (Davidson et al. 2003). Recent studies indicate
that the extraordinarily high abundance and
dominance of ants in certain habitats are closely
related to their lower trophic position: These ants
depend more on plant-based food sources, such
as extrafloral nectaries (EFNs) and honeydew
(Davidson et al. 2003, Wilder et al. 2011b). These
findings suggest that shifts in mutualistic interaction with hemipterans may have a considerable
impact on the population dynamics of ants in
nature (Davidson et al. 2003, Wilder et al. 2011b).
Ant-hemipteran interactions have a variety of
ecological effects on the host plants as well as on
other arthropods feeding on foliage (Styrsky and
Eubanks 2007, Zhang et al. 2012b). Ants can
reduce plant herbivory by consuming or driving
off other insects when tending hemipterans, but
this anti-herbivory effect is context-dependent
(Styrsky and Eubanks 2007, Zhang et al. 2012b).
Honeydew has a similar effectiveness when it
comes attracting ants and reducing herbivory
compared to EFNs (Fiala 1990, Chamberlain and
Holland 2009). Ant identity and abundance are
key factors determining the magnitude of the
protective effect; more ants often means greater
protection for plants (Moreira and Del-Claro
2005, Frederickson and Gordon 2009, Yamawo
et al. 2012). Nevertheless, the protective effect of
ants on plants can be saturated as ant abundance
increases (Palmer and Brody 2013). If shifts in
mutualistic interaction with hemipterans can
lead to varied ant abundance, it is reasonable to
predict that the herbivory level of the host plants
may also be impacted. Trophic position can be
used as an indicator for the dependence of ants
on the exudates of hemipterans, with a lower
trophic position indicating a tighter relationship
(Davidson et al. 2003, Wilder et al. 2011b).
Several recent studies have found that habitat
type, ecological corridor, logging, and species
invasion can lead to shifts in trophic position for
ants (Gibb and Cunningham 2011, Wilder et al.
2011b, Resasco et al. 2012, Woodcock et al. 2013).
However, the shifts in trophic position and
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corresponding ecological effects of ants along
environmental gradients have not been studied
previously.
How mutualistic interactions respond to the
changing world is one of the questions focused
on in ecology (Kiers et al. 2010). Despite the
ubiquity of ant-hemipteran interactions in many
communities, their macro-scale effects in varied
environments have received little attention (Styrsky and Eubanks 2007). Only recently two
experimental studies confirmed the negative
effects of warming on the ecological effects of
ant-aphid mutualism (Barton and Ives 2014a,
Marquis et al. 2014), and another two studies
evaluated the effects of ants on plants in large
scales (Hanna et al. 2015, Sendoya and Oliveira
2015). The effects of ant-aphid interactions under
environmental gradients are still far from clear.
Elevational gradients provide ‘‘natural experiments’’ for exploring shifts in interspecific interactions in varied environments (Korner 2007,
Sundqvist et al. 2013, Rasmann et al. 2014).
Numerous biotic and abiotic factors vary with
elevation, such as biodiversity, temperature, and
precipitation; this can lead to varied biotic
interactions (Sundqvist et al. 2013). Both ants
and their food sources can change with elevation
(Samson et al. 1997, Sanders 2002, Hodkinson
2005, Lach et al. 2010). Therefore, it is reasonable
to predict that the effects of ants on host plants
can also vary with elevation (Miller et al. 2009,
Lach et al. 2010).
Using aphid-mediated ant-plant interaction as
the study system, we aimed to explore the
association of ant trophic position, abundance,
and plant herbivory along an elevational gradient at Donglingshan Mountain in Beijing, China.
Based on our previous experimental work, the
aphid-tending ants Lasius fuliginosus can effectively reduce the herbivory level of the host plant
Quercus liaotungensis at the study site (Zhang et
al. 2012a). We hypothesized that along the
gradient: (1) Higher ant abundance should be
associated with a lower trophic position but a
higher abundance of aphids, and (2) higher ant
abundance should be associated with lower
levels of plant herbivory.
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MATERIALS
AND
the key food source attracting L. fuliginosus in the
canopy of Q. liaotungensis at the study site
(Zhang et al. 2012a).
METHODS
Study site
The study area, the Beijing Forest Ecosystem
Research Station of the Chinese Academy of
Sciences, is located at 40800 0 to 40803 0 N and
115826 0 to 115830 0 E. The area has a typically
warm, temperate, continental monsoon climate
with an average annual precipitation of 500–650
mm and a mean annual temperature of 5–108C.
The altitude of most of the area is over 1000 m
above sea level and peaks at 2303 m. The zonal
vegetation of the Donglingshan Mountain region
is a highly heterogeneous, warm temperate
deciduous broadleaf forest, and it mainly includes oaks (Q. liaotungensis), mixed tree species
(e.g., Tilia spp., Ulmus spp., Acer spp., Juglans
mandshurica, and Fraxinus rhynchophylla, among
others), birches (Betula spp.), and poplars (Populus davidiana). Some conifers and shrubs (e.g.,
Prunus spp. and Vitex negundo var. hetertophylla,
among others) are also present.
Survey of ant abundance
Pitfall traps were used to quantify the abundance of ants in the community in mid-July of
2010 and 2011. July is the middle of the growing
season and a highly active period for ants. Pitfall
traps are a sampling technique extensively used
to sample such surface-foraging invertebrates as
ants, beetles, and spiders (Cardoso et al. 2007,
Gonzalez-Megias et al. 2008, Wardle et al. 2011).
In each 10 3 10 m plot, three traps were set in a
triangular shape (with 5 m between vertices). If
there were ant nests in a plot, the traps were set
at least 2 m away from the nest, to avoid the
impacts of nest on the sampling. For each trap, a
cup (diameter ¼ 7.9 cm, depth ¼ 9.7 cm)
containing 50 ml of an alcoholic solution (5% in
concentration) was buried even with the soil
surface. Two days after the traps were set, we
retrieved the cups, and the samples were taken
back to the lab in order to identify the ants to
species and the abundance of each ant species
could be recorded.
Experimental design
At first, 10 western slopes dominated by Q.
liaotungensis were located in the study area.
Those 10 slopes form a single elevation gradient
that ranges from 1020 to 1770 m and that
completely overlaps the distribution range of Q.
liaotungensis in the study area (Qi et al. 2009).
Then, a transect was set up from the base to the
top of every slope in the study area. The width of
each transect was 10 m, with the length ranging
from 80 to 180 m. Along the gradient, the mean
annual temperature decreased about 4.78C, but
the mean annual precipitation increased about 84
mm (Qi et al. 2009).
Each transect was divided into 10 3 10 m plots,
resulting in a total of 119 plots. Plant herbivory
and ant abundance were surveyed in each plot.
Based on previous observations, L. fuliginosus
and Formica sinensis were the dominant ant
species in the study area. L. fuliginosus is a
typical honeydew-feeding ant and often nests in
the tree holes in the basal part of Q. liaotungensis
(Hopkins and Thacker 1999). Workers of L.
fuliginosus forage on both the ground and the
canopy of Q. liaotungensis. Aphids included
Lachnus tropicalis and Tuberculatus sp. in the
canopy and Stomaphis japonica on the trunk of
Q. liaotungensis (Zhang et al. 2012a). Aphids were
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Analysis of ant trophic position
Stable isotope analysis was used to estimate
the trophic position of ants. The nitrogen from
the tissue of consumers is enriched in dN15
relative to that of prey, which means that dN15 is
positively correlated with a consumer’s trophic
position (Post 2002). Ants in the middle portion
of each transect, within an area of approximately 10 3 50 m, were collected by hand. At each
transect, at least 30 individual ants were
collected as a sample, and three samples were
collected for each ant species within a transect.
For rarer species, we collected as many ants as
we could to create a sample. Herbivores (mainly
caterpillars) were collected from the canopy by
hand and by beating branches (Campos et al.
2006). Both ants and herbivores were immediately taken back to the lab and dried at 608C for
at least 48 hours until the weight of the sample
stabilized. Thereafter, we first removed the
abdomens of each ant to prevent recent stomach
contents from influencing dN15 values (Tillberg
et al. 2006, Wilder et al. 2011b); this approach
provides more relevant information about the
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long-term assimilation and incorporation of
nutrients from foods into tissues (Tillberg et al.
2006, Wilder et al. 2011b). Each sample was
ground with a mortar and pestle, and approximately 1 mg of each sample was packed into a
tin capsule for isotopic analysis. Samples were
analyzed for dN15 using a continuous-flow
isotope-ratio mass spectrometer (Finnigan Delta
V Advantage, Finnigan MAT, San Jose, California, USA). The d-value is expressed as d(%) ¼
(Rsample Rstandard)(Rstandard)1 3 1000%, where
Rsample and Rstandard refer to the molar ratios of
the heavier isotope to the lighter isotope
(15N/14N) of the sample and the standard molar
ratio (which corresponds to atmospheric air).
The isotope ratio of herbivores was used as a
baseline (trophic position ¼ 2) to predict the
trophic position of ants (Wilder et al. 2011b). The
trophic position of ants was calculated as
follows: trophic position ¼ (d15aN d15hN)/3.4
þ 2, where d15a N is the value for ants, and d15h
N is the value for herbivores. According to a
previous review, the mean enrichment in d15N
for one consumer trophic-level transfer was set
as 3.4 (Post 2002).
for ants in the community; they provide ants
with honeydew and other food sources (Zhang et
al. 2012a). In the middle portion (approximately
10 3 50 m) of each transect, we surveyed 30
randomly selected trees and recorded whether or
not there were ants active on the trees. Observations were conducted between 9:00 a.m. and 4:00
p.m., which is a highly active period for ants, on
a sunny day. If ants were active on a tree, we
assumed that the tree was occupied by ants. The
proportion of trees occupied by ants (PTOA) and
the species of ants were recorded. All of the
above samples were collected in mid-July of
2011.
Data analysis
The data for herbivory and the abundance of
ants and aphids were log-transformed to conform to the assumptions of parametric analysis.
Ordinary regression was used to fit the variation
in different variables along the elevational
gradient. The averaged value of each plot was
used to fit the relationship between the averaged
herbivory and ant abundance by a linear mixed
effect model. To account for possible heterogeneity among transects, different transects were
allowed to have varied variances in the model.
A Kenward-Roger approximation was used to
adjust the degrees of freedom. Model diagnosis
was also conducted by fitting residuals with
predicted values and testing the normality of the
residuals. The relationship between aphid and
ant abundances was also analyzed using this
model.
Only the ant abundance middle portion of
each transect (within an area of approximately 10
3 50 m) was used to fit the relationship between
ant abundance and ant trophic position, as the
ants used in isotope analysis were collected in
this area. Considering the small sample sizes for
trophic position and PTOA (with each transect
having only one data point), simple linear
regression was used to evaluate the relationship
between the two variables as well as their
relationship with ant abundance. In addition to
the linear regression, a randomization test was
used to test the relationship between trophic
position and PTOA, with a re-sampling of 1000
times. The Kruskal-Wallis test was employed to
explore the difference in ant trophic position
between transects with only one species and
Survey of plant herbivory, aphid abundance,
and the occupation of food sources by ants
To investigate plant herbivory, we randomly
selected three trees of Q. liaotungensis in each
plot. On each tree, a twig was cut off from a
south-facing branch 4–5 m in height. To prevent
leaf-selection bias, the first to sixth leaves were
collected from the tip of each twig. To examine
aphid abundance, we cut off another twig 4–5 m
in height on each tree and recorded the number
of aphids found from the tip of the twig to the
10th leaf. For the herbivory analysis, all of the
leaves were scanned using an EPSON Perfection
4870 Photo flatbed scanner (EPSON America,
Inc., USA) and then used to determine the degree
of herbivory. For each leaf, the gaps in the
scanned leaf image (herbivore damage) were
filled in Adobe Photoshop CS2 (Adobe Systems
Inc., USA), according to the expected shape. The
area of the original (a) and repaired (b) leaves
was calculated using WinFOLIA Basic 2004a
(REGENT Instruments Inc., Australia). The percentage of leaf-area loss was calculated as
follows: L (%) ¼ (b a)/b 3 100.
Q. liaotungensis trees are the main host plants
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transects in which more than one species had
been found. To fully analyze the relationship
among ant trophic position, the proportion of
trees occupied by ants, ant/aphid abundance, and
plant herbivory, a partial correlation among these
variables was conducted, with altitude as the
partial parameter. All analyses were conducted
using SAS 9.2.
elevation, with 20.39% of the variation explained
by elevation (Fig. 1D). Among the 10 transects,
the mean level of plant herbivory varied from
3.89% to 14.99%. The pattern of the proportion of
trees occupied by ants was similar to the pattern
of ant abundance as well as that of aphid
abundance, with a peak at middle elevations
(Fig. 1E).
In light of the widespread distribution (in nine
of the 10 transects) and dominance of L.
fuliginosus along the gradient, only the data for
this species were used for analyses related to
trophic position. The trophic position of L.
fuliginosus ranged from 2 to 3 among different
transects, indicating that this species is omnivorous and thus feeds on both plant- and animalbased food sources. The trophic position of L.
fuliginosus showed no clear trends with elevation
(Fig. 1F).
RESULTS
Variation in different variables
along the elevational gradient
Along the elevational gradient, ant abundance
for the two years had a significant positive
relationship (R 2 ¼ 85.9%, P , 0.0001); a further
analysis found that year had no effect on ant
abundance, and neither did the interaction
between year and elevation (both P . 0.4). The
data for the two years were thus pooled for the
analysis. In total, 34 549 worker ants were
collected. There was a large variation in ant
abundance in different transects: The total ant
abundance varied approximately 87 times, and
the dominant ant species L. fuliginosus varied
approximately 250 times in abundance.
L. fuliginosus contributed 87.18% of the total
ant abundance and was found in nine of the 10
transects. The red wood ants, F. sinensis, contributed to 8.25% of the total ant abundance. Several
other species were found in very low abundance,
including Camponotus japonicus Mayr, Formica
fusca Linnaeus, and Tetramorium caespitum. Only
in one transect (T3) were no workers of L.
fuliginosus collected. In this transect, the dominant species was the highly aggressive red wood
ant F. sinensis. This ant species monopolized the
transect with a high abundance (mean ¼ 54.24
workers per trap, se ¼ 11.05, n ¼ 49), and no other
ant species was collected via pitfall trap sampling.
Ant abundance peaked at middle elevations,
and more than half of the variation in ant
abundance was explained by elevation (Fig.
1A). For L. fuliginosus, elevation explained
48.22% of the variation in its abundance (Fig.
1B). The pattern of aphid abundance was similar
to that of ants, with more than 60% of the
variation explained by elevation (Fig. 1C).
Plant herbivory tended to decrease with
elevation at first, and then it increased with
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Association among ant trophic position,
abundance, and plant herbivory
Among the different transects, a higher abundance of L. fuliginosus was associated with a
lower trophic position and higher abundance of
aphids. More than 20% of the variation in ant
abundance at the middle portion of each transect
can be explained by shifts in trophic position
(Fig. 2). A clear bias in the residuals of the mixedeffect model was detected when the relationship
between the abundances of ants and aphids was
evaluated. This model was instead tested by
linear regression. Aphid abundance explained
nearly half of the variation in the abundance of L.
fuliginosus (Fig. 2). The trophic position of L.
fuliginosus was significantly lower in transects in
which only this ant species was found than in
other transects in which several species coexisted
(Chi-square ¼ 5.4, df ¼ 1, P ¼ 0.02; Fig. 1F).
Furthermore, compared to transects in which
several ant species coexisted, ant abundance was
significantly higher in transects in which only L.
fuliginosus was found (F1,43 ¼ 556.58, P , 0.0001).
The trophic position decreased with the proportion of trees occupied by ants. The proportion
of trees occupied by ants explained 49.93% (P ¼
0.03) of the variation in trophic position (P ¼
0.032 for the randomization test; Fig. 3). Ant
abundance and the proportion of trees occupied
by ants also had a tight positive relationship (R 2
¼ 78.25%, P , 0.0001).
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Fig. 1. The variation of different variables along the elevational gradient. (A) the total ant abundance; (B) the
dominant ant species L. fuliginosus; (C) the aphid abundance on the leaves of Q. liaotungensis; (D) leaf herbivory
for Q. liaotungensis; (E) the proportion of trees occupied by ants on each transect, elevation increases from T1 to
T10; (F) the trophic position of L. fuliginosus at each transect, elevation increases from T1 to T10; red dashed lines
represent 95% confidence interval. For (F), blank bars represent transects that were monopolized by L. fuliginosus
and grey bars represent transects where several ant species coexist.
ant abundance was more clear at the transect
scale: The total ant abundance could explain
about 58% of the variation in herbivory among
different transects (P ¼ 0.0106 ), while the
abundance of L. fuliginosus itself could explain
47% of the variation (P ¼ 0.041; Appendix: Fig.
A1). When the effect of altitude was controlled,
the relationship between different variables was
Plant herbivory decreased linearly with the
total abundance of ants (F1,53.2 ¼ 31.34, P ,
0.0001), and nearly 20% of the variation in
herbivory can be explained by ant abundance
(Fig. 4A). The abundance of L. fuliginosus itself
could explain 14% of the variance for plant
herbivory (F1,47.6 ¼ 17.01, P , 0.0001, Fig. 4B).
The negative relationship between herbivory and
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Fig. 2. The relationship between the abundance and trophic position of L. fuliginosus (A) and the abundances of
ants and aphids (B). Red dashed lines represent 95% confidence interval.
still significant except for that between trophic
position and herbivory (Table 1).
DISCUSSION
Exploring how biotic interactions and their
ecological effects change in varied environments
is one of the key focuses of ecological studies
(Sundqvist et al. 2013). With this observational
study, we show that spatial variation in ant
trophic position, abundance, and plant herbivory
are closely related. These results suggest that
shifts in the mutualistic interaction between ants
and aphids can account for the variation in ant
abundance and its ecological effect across a
continuous environmental gradient.
Our results suggest that shifts in the strength
of ant-aphid interactions may be a key factor in
Fig. 3. The relationship between trophic position, ant
abundance and the proportion of trees occupied by
ants. Red dashed lines represent 95% confidence
interval.
Fig. 4. The relationship between the herbivory of Q. liaotungensis and the total ant abundance (A) and the
abundance of L. fuliginosus (B). Red dashed lines represent 95% confidence interval.
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Table 1. The partial correlation between ant/aphid abundance, herbivory the trophic position of ants and the
proportion of trees occupied by ants (PTOA); * represents significant correlation (P , 0.05).
Variable
Ant abundance
Herbivory
Trophic position
PTOA
Aphid
Ant abundance
Herbivory
Trophic position
PTOA
Aphid
1
0.3408*
1.0000
0.6923*
0.1262
1.0000
0.8842*
0.2943*
0.8428*
1.0000
0.7873*
0.3157*
0.7326*
0.8356*
1.0000
the spatial population dynamics of ants across
different environments. In lowland tropical
forests, higher ant abundance is associated with
a lower trophic position (Davidson et al. 2003).
Our study suggests that for ants, the negative
relationship between abundance and trophic
position may be a common phenomenon in
different terrestrial ecosystems rather than being
restricted to tropical areas. In our study, the
plant-based foods used were mainly honeydew
secreted by aphids (Zhang et al. 2012a). Several
previous studies found that feeding on more
plant-based foods, such as honeydew, can effectively enhance the growth rate (Wilder et al.
2011a), competitive ability (Heil 2008, Wilder et
al. 2011b) and even the immunity of the ant
colony (Kay et al. 2014). We found that at the
community level, food source occupation and
interspecific competition can be closely related to
the trophic position and abundance of ants along
the elevational gradient. At the three transects
monopolized by L. fuliginosus, their trophic
position was significantly lower, but their abundance was higher than it was in the other six
transects in which several ant species coexisted.
These results suggest that a more intimate
interaction with aphids can not only enlarge the
population size but also can enhance the ants’
competitive ability in varied environments.
We suggest that the effect of biotic defense
should not be neglected when accounting for the
variation in herbivory across larger spatial scales
(Moles et al. 2011, Andrew et al. 2012). A
previous study found that the leaf traits of Q.
liaotungensis varied with elevation in our study
area, but none of the patterns were similar to the
elevational patterns of herbivory (Qi et al. 2009).
Therefore, it is unlikely that the pattern of
herbivory is largely determined by leaf traits
rather than ants along the elevational gradient.
According to the resource availability hypothesis,
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herbivory should decrease with elevation because in nutrient poor environments (such as
higher elevations), plants should invest more in
defense against herbivores (Coley et al. 1985), as
several recent studies found (Miller et al. 2009,
Garibaldi et al. 2011, Metcalfe et al. 2014,
Rasmann et al. 2014). However, our results show
that plants at middle elevations have the lowest
levels of herbivory, and we suggest that the
variation in ant abundance may be an important
determining factor in this pattern. More ants can
provide plants with stronger protective effects
(Oliveira et al. 1999, Heil et al. 2001, Yamawo et
al. 2014). In our study, at higher elevations,
where ant abundance was lower, the mean value
of herbivory reached nearly 15%; however, at
middle elevations, where ant abundance was
higher, the value fell below 6%. For oaks, an
herbivory level of more than 8% can significantly
decrease the production of fruit (Crawley 1985).
We suggest that the weaker protective effect of
ants may be an important factor limiting the
fitness of Q. liaotungensis at higher elevations. At
lower elevations (from 1000 to 1400 m), opposite
patterns between ant abundance and herbivory
were also detected, suggesting the anti-herbivory
effect of ants is also important in this area. We
noticed that in general, compared to plants at
lower elevations (,1400 m), plants at higher
elevations (.1400 m) suffered higher levels of
herbivory. The explicit mechanism underlying
this pattern is unclear, but it is possible that at
higher elevations, plants are more subject to
herbivory. This is because in these stressful
habitats, plants are limited in their ability to
compensate for herbivory in accordance with the
prediction of the compensatory continuum model (Appel and Cocroft 2014). Compared to higher
elevations, plants at lower elevations may have
higher levels of constitutive defense (Rasmann et
al. 2014). This can partially explain why both
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plants (Barton and Ives 2014a, b, Marquis et al.
2014). In this study, we found there was a closer
relationship between ants and aphids at sites at
middle elevations, where the temperature and
precipitation were also at an intermediate level
(Qi et al. 2009). Thus, the suitable environments
for ant-aphid mutualism may shift upward in the
context of global warming.
In conclusion, through an observational study
along an elevational gradient, we found that antaphid mutualism may be an important factor
influencing the spatial variation in ant abundance and plant herbivory at a relatively larger
spatial scale. The study suggests that the importance of biotic interactions in mediating certain
key ecological processes and patterns in varied
environments should not be neglected. It should
be addressed that the observational nature of this
study limits the confirmation of a mechanistic
link between different patterns we found. Experimental studies are still needed to pinpoint the
specific mechanisms causing the variance of
mutualistic interactions in varied environments.
ACKNOWLEDGMENTS
This work was supported by National Natural
Science Foundation of China (31300368, 31370451).
We thank Zhenghui Xu and Gexia Qiao for ant- and
aphid-species identification. S. Zhang and Y. Zhang
contributed equally to this work.
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SUPPLEMENTAL MATERIAL
ECOLOGICAL ARCHIVES
The Appendix is available online: http://dx.doi.org/10.1890/ES15-00229.1.sm
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