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Phil. Trans. R. Soc. B (2012) 367, 3115–3124
doi:10.1098/rstb.2011.0346
Research
Climate change effects on above- and
below-ground interactions in a
dryland ecosystem
Adela González-Megı́as1, * and Rosa Menéndez2
1
Depto. de Zoologı́a, Facultad de Ciencias, Universidad de Granada, 18071 Granada, Spain
2
Lancaster Environment Centre, Lancaster University, Lancaster, LA1 4YQ, UK
Individual species respond to climate change by altering their abundance, distribution and phenology. Less is known, however, about how climate change affects multitrophic interactions, and its
consequences for food-web dynamics. Here, we investigate the effect of future changes in rainfall
patterns on detritivore– plant – herbivore interactions in a semiarid region in southern Spain by
experimentally manipulating rainfall intensity and frequency during late spring – early summer.
Our results show that rain intensity changes the effect of below-ground detritivores on both plant
traits and above-ground herbivore abundance. Enhanced rain altered the interaction between detritivores and plants affecting flower and fruit production, and also had a direct effect on fruit and seed
set. Despite this finding, there was no net effect on plant reproductive output. This finding supports
the idea that plants will be less affected by climatic changes than by other trophic levels. Enhanced
rain also affected the interaction between detritivores and free-living herbivores. The effect, however, was apparent only for generalist and not for specialist herbivores, demonstrating a
differential response to climate change within the same trophic level. The complex responses
found in this study suggest that future climate change will affect trophic levels and their interactions
differentially, making extrapolation from individual species’ responses and from one ecosystem to
another very difficult.
Keywords: precipitation; detritivores; free-living insects; seed predators; trophic interaction;
semiarid environment
1. INTRODUCTION
Climate change is having a strong impact on biological
systems through changes in species populations, communities and ecosystem processes, with potential
consequences for future ecosystem provision [1–4].
A major challenge for ecologists is, therefore, to predict
the magnitude and consequences of future climate conditions for all of the above levels of biological complexity
[5,6]. The effect of recent climate change is already
evident at the level of species abundance and distribution [2–4,7], with many species throughout the
world shifting their latitudinal and altitudinal ranges
consistent with the recorded warming [3–5,7–10].
These range changes caused colonization and extinction
events that have resulted in changes in the diversity
and composition of communities [10–12]. The relative
abundance of species within communities is also changing, with increasing dominance by newly arriving
* Author for correspondence ([email protected]).
Electronic supplementary material is available at http://dx.doi.org/
10.1098/rstb.2011.0346 or via http://rstb.royalsocietypublishing.org.
One contribution of 10 to a Theme Issue ‘Impacts of global
environmental change on drylands: from ecosystem structure and
functioning to poverty alleviation’.
species and species with broad ecological niches at the
expense of species with narrow environmental/habitat
requirements [9,10]. In addition, phenological changes
in plant and animal species in response to climate
change have been widely reported [4,13–15].
Despite the accumulating evidence of individual
species responding to climate change [16,17], little
empirical information exists on the effect of climate
change on species interactions [6,18,19]. Species
vary in their individual response to climate change
that may lead to the disruption in both antagonistic
[20,21] and mutualistic interactions between species
[22,23]. Stronger disruptions are likely to occur if
the sensitivity to climate change differs not only
between species, but also between trophic levels
[18,19,24,25]. Crucially, the disruption of these interactions can affect food-web dynamics and evolutionary
processes [16,17,19,26].
In terrestrial ecosystems, the interaction between
herbivores and plants is known to be affected by
changing climatic conditions because each group
responds differently to environmental factors [27,28],
and therefore the strength and outcome of their interactions are likely to be affected by climate change [27].
For example, a recent review of the potential effects of
climate change on arthropod – plant interactions shows
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A. González-Megı́as and R. Menéndez
Climate change and trophic interactions
that the interactive effect of CO2 and temperature provokes an increase in the rate of herbivory, owing to a
reduction in the defensive secondary metabolites produced by the plants [28]. Terrestrial plant-based
food webs also involve below-ground organisms intimately connected to above-ground organisms [29–
31] and differentially affected by climatic conditions
[32– 34]. For example, air temperature shows higher
variation than soil temperature, owing to the wellknown damping effect of soil. This suggests that climatic conditions are likely to change more abovethan below-ground in the near future [35]. As a
result, a potential mismatch between above- and
below-ground interactions and processes is likely to
occur [26,33,34].
Our poor understanding of the effects of climate
change on species interaction and food-web dynamics
is also exacerbated by the lack of studies exploring the
effect of climate change on key components, such as
decomposers, of terrestrial food webs [36,37]. In the
case of decomposers, this is despite decomposers
being important and abundant members of most
food webs, interacting with plants and affecting other
members of the community [29– 31]. Their activity
enhances microbial turnover, nutrient recycling and
the breakdown of organic matter, favouring plants in
many ways [29,38]. Multiple ecosystem processes
should therefore be explored in parallel because,
despite all processes being intimately interconnected,
some of them might be more sensitive than others to
different components of climate change.
The outcome of species interactions and their
responses to climate change are not only species-dependent, but also habitat-dependent. Simple habitats are
expected to be less stable than more complex habitats
[39], and therefore a stronger response to variation in
climatic conditions would be expected. Arid and
semiarid ecosystems are characterized by relatively low
biodiversity in terms of both species and interactions.
They are also especially sensitive to changes in rainfall
[40], but see [41]. General circulation models project
a reduction in precipitation and an increase in temperature in Mediterranean areas over the coming decades
[42]. However, while temperature is clearly expected
to increase, changes in rainfall patterns are likely to be
seasonal [43,44]. These models project a potential
increase on the frequency of early summer rains, and
a reduction of precipitation in winter and autumn
[42,43]. Therefore, projected changes in rainfall patterns in southern Europe are likely to affect plant
growth, primary productivity and nutrient availability
[45–47], but also species interactions [48,49]. Few
studies, however, have examined the effect of rainfall
alteration on animal and plant species in arid or
semiarid ecosystems [50].
Here, we investigate detritivore– plant – herbivore
interactions, testing the potential effect of a future climatic scenario on the fate of these interactions in a
semiarid region in southern Spain. We experimentally
manipulate rainfall intensity and frequency during late
spring– early summer period in order to discern the
potential effects of changing rainfall patterns on tritrophic interactions that involve above-ground and
below-ground organisms.
Phil. Trans. R. Soc. B (2012)
2. MATERIAL AND METHODS
(a) Study system
The study was conducted in 2011 at Barranco del
Espartal, a seasonal watercourse located in the arid
Guadix-Baza Basin (Granada, southeastern Spain).
The climate is continental Mediterranean with strong
temperature fluctuations (ranging from 2148C to
408C) and high seasonality (hot summers, cold winters).
The soil is characterized by a sandy–loam texture, high
pH, low water-retention capacity and high salinity. As
generally found in arid soils, most of the ground surface
is devoid of plant litter (58%), which appears only
under shrubs and in ant-nest mounds. The vegetation is
an arid open shrub-steppe dominated by Artemisia
herba-alba Asso, A. barrelieri Bess. (Asteraceae), Salsola
oppositifolia Desf. (Salsoloideae), Stipa tenacissima
L. (Poaceae), Lygeum spartum L. (Poaceae) and Retama
sphaerocarpa L. (Fabaceae). The short-lived Brassicaceae
species Moricandia moricandioides (Boiss.) Heywood is
highly abundant in this habitat and as a result, was used
as a model system. Moricandia moricandioide’s plants are
distributed in monospecific stands, and no litter accumulates underneath the plants owing to their small size. This
species grows as a vegetative rosette during winter, and
produces reproductive stalks during spring. The stalks
remain photosynthetically active during the entire season.
The insect herbivores associated with M. moricandioides include specialist and generalist chewers [51].
The most abundant specialists are the pierids Pontia
daplidice L., Euchloe crameri Batler and Pieris rapae
L., the diamondback moth (Plutella xylostella L.,
Plutellidae) and the sawfly Tenthredo sebastiani Lacourt
(Hymenoptera, Tenthredinidae). Generalist chewers
include various species of grasshoppers and beetles.
Sapsuckers are also abundant in the study area,
mainly represented by the specialist aphids Brevicoryne
brassicaceae (Linnaeus, 1758) and Lipaphis erysimi
Kaltenbach, and the generalists: the aphid Myzus persicae Sulzer and the planthopper Agalmatium bilobum
Fieber (Hemiptera, Issidae). The most abundant
seed predator species (found in 99% of fruits) on M.
moricandioides is Crossobela trinotella (Herrich-Schäffer,
1856; Lepidoptera, Gelechiidae).
Below-ground organisms such as Morica hybrida
Charpentier (Coleoptera: Tenebrionidae) and Cebrio
gypsicola Graells (Coleoptera: Cebrionidae) are among
the most abundant generalist detritivores and root herbivores, respectively, to be found in the study area [52].
The above- and below-ground organisms associated
with M. moricandioides affect the induction of defensive
chemical compounds by the plant and also affect each
other through complex interactions [51].
(b) Experimental set-up
To explore the individual and combined effect of detritivores and a future climate change scenario on the
interaction between the model plant species and the
above-ground insects, we conducted an experiment
in the field in 2011. The experiment was a split-plot
design with two factors with two levels per factor.
The two factors were: climate change, in which
summer rainfall precipitation was altered (climate
change hereafter), and detritivores, in which the
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Climate change and trophic interactions A. González-Megı́as and R. Menéndez
presence/absence of this guild was manipulated (detritivores hereafter). The climate change treatment was
applied to 12 randomized blocks. Each block had 10
plants located in three lines (3 þ 3 þ 4 plants per line),
and at least 30 cm apart from each other (120 plants
in total). During the winter of 2010–2011, seeds of
M. moricandioides, collected from the study area, were
germinated in pots with soil from the study area and
grown in a common garden. The plants were kept in
these pots until mid-May (16 May 2011) when they
were moved to the field. Plants were re-potted using
mixed soil (free of macroarthropods) from the study
site. The pots consisted of fibre-glass-mesh cylinders
(10 15 cm) of 1 mm mesh size to inhibit the entrance
or escape of detritivores. These pots were then buried
with the upper surface level with the ground. During
the first week in the field, and in the absence of natural
rain, all plants were watered to ensure their establishment. None of the plants had a reproductive stem at
the moment of being moved to the field.
The climate change treatment has two levels (six
blocks per level): enhanced summer rainfall (rain)
and control, with no manipulation. The rain level
simulated a climate change scenario in which precipitation during the summer is increased compared
with current conditions, but it is concentrated in a
few events (lower frequency). To do so, we calculated
the mean precipitation that occurred in the study area
in the last 10 years for two periods: (i) the beginning of
spring (March– April) and (ii) late spring to the beginning of summer (May– June; electronic supplementary
material, table S1). We also calculated the mean precipitation in June and July for the same historical
period (see the electronic supplementary material,
table S1). We supplemented precipitation in June by
adding sufficient water to increase precipitation to
the mean precipitation obtained for the first period
(March– April). In a similar way, we simulated an
increase in precipitation in July by supplementing it
to the level of the mean of the second period (May–
June). The frequency of the rain events was also
reduced by approximately 50 per cent. The enhanced
rainfall was applied four times in June and twice in July
to simulate the amount of rainfall but concentrated in
fewer events compared with natural spring rainfall (see
the electronic supplementary material, table S1).
August was not included in the experiment because
no plants survive (in natural or under experimental
conditions) to this month. To simulate cloud cover
during the experimental rain events, we covered the
blocks with a net that filtered radiation by 50 per
cent. This net was used during the day of the experimental rain event, and the day after, simulating the
mean reduction of solar radiation that has been
observed under natural rain conditions in the study
area during the last 10 years.
The detritivores treatment consisted of two levels:
the addition of one larva of the tenebrionid M. hybrida,
and the control with no detritivore. Each of the 10 pots
within each block was allocated randomly to one of two
detritivore levels. One third-instar larva of the detritivore M. hybrida was added to the soil of each plant
assigned to that treatment. The tenebrionid larvae
were collected from the study area during the spring.
Phil. Trans. R. Soc. B (2012)
3117
(c) Data collection
To score free-living herbivores, the number of naturally occurring sapsucker and chewer herbivores was
recorded on each experimental plant every three days
after the set-up of the experiment (15 May 2011).
Total abundance of each herbivore guild was calculated by summing the number of individuals
recorded during all the surveys until the end of the
experiment (end of July). To avoid problems of summing individuals counted in a previous census, we
subtracted at each census the number of individuals
of the same instar/type (winged versus not winged)
counted in the previous census. We also counted the
number of eggs laid by pierid species (Lepidoptera)
on leaves and flowers.
At the end of the experiment (28 July 2011), we
measured plant height and the diameter of the main
stem, and counted the number of reproductive stems
and the total number of flowers and fruits produced
by each plant. Fruits were collected after complete
maturation of seeds but before seed dispersal. Fruits
were carried to the laboratory where the total
number of seeds per plant was estimated by multiplying the number of fruits per plant the average
number of mature seeds per fruit found in 10 fruits
per plant. The number of ovules, aborted seeds and
predated seeds were also counted. When the number
of fruits per plant was equal to or less than 10, the
number of seeds per fruit was counted in all fruits of
the plant. Fruit set was calculated as the proportion
of flowers that passed to fruits, and the seed set as
the proportion of ovules that produced seeds per ripe
fruit. The abundance of seed predators was quantified
by counting the total number of fruits with at least one
predator. This is a conservative estimate of seed predator abundance because it is possible to find up to
three seed predators per fruit [51]. The attack rate of
seed predators was calculated as the proportion of
fruits infested by seed predators.
All the above-ground part of the plants was collected
individually from the field and oven-dried at 408C
for 72 h (until complete desiccation). Above-ground
tissue was weighed to calculate above-ground biomass.
C and N concentrations, and their ratio in aboveground tissue were determined for each plant using a
CHN Elemental Analyzer (CIC, Univ. Granada).
(d) Statistical analyses
Linear (LMM) and generalized linear-mixed models
(GLMMs) were used to test the effects of each factor
(climate change and detritivores) and their interaction
on herbivore abundance and plant traits. Block was
included in all the analyses nested within climate
change, and as a random factor to control for the
potential effect of the location. LMMs were used for
variables fitting a Gaussian distribution. GLMMs
were used for variables fitting binomial distribution
(with logit as link function) and Poisson distributions (with log as link function). Where overdispersion
was found, we ran the GLMMs with individual-level
variability, which allows for variation at the individual
rather than at the group level (including individuals as
a random factor). All analyses were performed on R
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Phil. Trans. R. Soc. B (2012)
4.29
3.37
6.67**
0.01
0.71
0.24
4.42
0.01
0.88
0.001
0.32
0.75
CC
D
CC D
1.25
0.45
1.57
1.10
4.28***
27.31***
0.53
3.86***
26.88***
4.47ms
2.48
0.09
17.76**
0.19
1.07
0.10
0.80
1.98
F
F
F
F
F
F
C/N tissues
plant biomass
N seeds
seed set
fruit set
N fruits
z
z
z
F
model
(b) Effects of the experiment on plant traits
There was a significant effect of the interaction between
detritivores and climate change on plant traits (table 1;
see electronic supplementary material, table S2), with
detritivores negatively affecting flower and fruit productions in the rain level (figure 1). There was no
effect of detritivores or climate change on the number
N flowers
3. RESULTS
(a) Above-ground insect assemblage associated
with Moricandia moricandioides
During the study period, several species of generalist
and specialist chewer and sapsucker insects visited
and fed on the experimental plants. We found 1.98 +
0.16 specialist chewers/plant belonging to four species:
Euchloe crameri, E. belemia (Esper), Pontia daplidice and
Plutella xyllostella. Generalist chewers were in general
less abundant (0.34 + 0.06 generalist chewers per
plant), and 96 per cent of them belonged to three
species of beetles; Galeruca angusta (Kuster), Mylabris
quadripunctata (L.) and Mylabris hieracii (Graells), and
two unidentified species of Orthoptera (only immature
individuals were recorded).
Four species of sapsuckers represented 99 per cent of
all the individuals found in the census. These consisted
of two specialists—Brevicoryne brassicacea, and Lipaphis
erysimi (4.26 + 1.67 individuals per plant)—and two
generalists—Agalmatium bilobum and an unidentified
species of cicadellid (12.21 + 0.92 individual per plant).
N stems
program [53], using the lme4 package [54]. GLMMs
were fitted and evaluated with a log-link function
with the Laplace approximation [55]. The z-value
for each of the factors in the GLMMs is shown with
the results. The z-value is not reliable enough to be
used to assess the significance of the module; so it is
used in this study only to compare the relative importance of each variable. To solve this problem, we follow
the recommendation suggested by Bolker et al. [55],
and the fixed factors were tested in GLMMs by the
information-theoretic approach [56]. The approach
compares the fits of a suite of candidate models
using Akaike’s information criterion (AIC). This is
carried out by comparing the AIC of a model including only the intercept against the models built by
including each fixed factor every time (with the
random equation complete). We used the secondorder AIC, AICc as recommended by Burnham &
Anderson [56]. AICc differences (Di) were calculated
for each model (AICi – AICmin), which provides a ranking of the candidate models. The larger the AIC
difference for a model, the less probable that it is the
best model. As a rough rule of thumb, it has been proposed that models for which Di 2 receive substantial
support and are considered when making inferences,
that models having 4 Di 7 have considerably less
support, and that models having Di . 10 receive no
support [56]. Following this recommendation, only
models with Di 2 were selected in this study. We calculated the AICc weight (wi) for each candidate
model, the wi sum to 1, which indicates the probability
that model i is the best model.
The mean + s.e. is shown throughout the manuscript.
C/N seeds
Climate change and trophic interactions
plant height
A. González-Megı́as and R. Menéndez
Table 1. Results of the linear-mixed models (F provided) and generalized mixed model (z provided, see §2) for the effect of climate change (CC) and detritivore (d) treatments on
Moricandia moricandioides reproductive output. Block was included as a random factor nested on climate change. ms, .0.05 2 ,0.07; *,0.05; **,0.01; ***,0.001.
3118
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28
18
26
17
24
16
22
15
20
*
18
16
14
C/N in seeds
N flowers
Climate change and trophic interactions A. González-Megı́as and R. Menéndez
3119
*
14
13
12
12
11
10
10
9
control
12
N fruits
10
8
*
6
4
2
control
rain
Figure 1. The effect of climate change (control and rain
levels) and detritivores (Dþ denotes presence (filled circles),
D2 denotes absence (open square)) treatments on the
number of flowers and fruits produced by Moricandia
moricandioides. Mean + s.e. are shown. n ¼ 104 plants.
of reproductive stems produced by the plants, on plant
height or on above-ground biomass (table 1).
Climate change affected fruit set and seed set in
opposing ways (table 1), with less fruit set in the rain
level than in the control level (rain: 0.29 + 0.04
versus control: 0.39 + 0.04), and more seed set in
the rain level than in the control level (rain: 0.32 +
0.04 versus control: 0.18 + 0.03). The treatments in
our experiment did not affect the total number of
seeds produced by the plants (table 1).
A significant effect of the interaction between detritivores and climate change was also observed when
comparing seed quality (quantified as C/N ratio;
table 1), with detritivores reducing seed quality in
the control level, and increasing seed quality in the
rain treatment (in the rain treatment, the difference
between the level of detritivores was only marginally
significant; figure 2). Our treatments did not affect
the quality of the above-ground tissue (table 1).
(c) Effects of the experiment on above-ground
herbivores
Detritivores reduced the abundance of sapsuckers by
28 per cent, and the abundance of specialist sapsuckers by 45 per cent (see table 2 and electronic
supplementary material, table S2). There was a significant effect of the interaction between detritivores and
climate change on generalist sapsuckers (see table 2
and electronic supplementary material, table S2),
with detritivores negatively affecting generalist sapsuckers in the rain level (figure 3a). No significant
interaction effect between treatments was found on
Phil. Trans. R. Soc. B (2012)
rain
Figure 2. The effect of climate change (control and rain
levels) and detritivores (Dþ denotes presence (filled circles),
D2 denotes absence (open square)) treatments on C/N ratio
in the seeds of Moricandia moricandioides. Mean + s.e. are
shown. n ¼ 68 plants.
the abundance of all sapsuckers or specialist sapsuckers (see table 2 and electronic supplementary
material, table S2).
Detritivores reduced the abundance of chewer herbivores by 27 per cent, although the effect was only
marginally significant, and the abundance of specialist
chewers by 28 per cent with no interaction effect of
detritivores and climate change (see table 2 and electronic supplementary material, table S2). There was,
however, a significant effect of the interaction between
detritivores and climate change on the abundance of
generalist chewers (table 2), with detritivores negatively affecting generalist chewers in the rain level
(figure 3b). Neither detritivores nor climate change
affected the number of eggs laid by pierid butterfly
species (table 2).
There was a significant effect of the interaction
between detritivores and climate change on seed predator abundance (table 2), with detritivores increasing
the abundance of seed predators by 57 per cent in
the control level, and decreasing seed predator abundance by 37 per cent in the rain level (figure 4).
Detritivores also increased seed predator attack rate
by 47 per cent in the control level (figure 4), with
the detritivores and climate change interaction effect
being marginally significant (table 2). The mean
number of predated seeds per fruit was 6.95 + 0.99,
with no significant effect of our treatments (table 2).
4. DISCUSSION
Our results show that changes in rainfall had a strong
effect on trophic interactions in the M. moricandioides
system, owing to differences in the response of each
trophic level to the simulated rain events.
Our experiment revealed a strong effect of the interaction between climate change and detritivores
treatments on plant traits, with rain alteration affecting
fruit and seed set, but with no net effect on the reproductive output of the plant. The combined effect of
climate change and detritivores on plants was neutral
in terms of the total number of seeds produced by
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A. González-Megı́as and R. Menéndez
Phil. Trans. R. Soc. B (2012)
Climate change and trophic interactions
20
generalist sapsuckers
0.07
0.50
1.65
16
14
12
10
*
8
6
0.01
0.37
3.28ms
F
18
F
seed p. attack
rate
predated seed per
fruit
(a)
4
generalist chewers
0.60
0.36
4.39*
0.03
1.07
24.05*
F
0.6
F
generalist
chewers
seed
predators
(b) 0.7
0.5
0.4
0.50
22.13*
0.32
0.78
0.64
0.30
CC
21.39
D
26.26***
CC D 21.46
20.69
27.83***
1.41
21.09
22.33*
23.02**
0.66
21.76ms
20.44
z
z
z
z
z
z
model
specialist
chewers
N egg S
chewers
chewers
generalist
sapsuckers
specialist
sapsuckers
*
0.3
0.2
0.1
0
sapsuckers
Table 2. Results of the linear-mixed models (F provided) and generalized mixed model (z provided, see §2) for the effect climate change (cc) and detritivore (D) factors on the
abundance of herbivores associated to Moricandia moricandioides. Result for the number of eggs laid by specialist butterfly species (N egg S chewers), seed predator attack rate (seed
p. attack rate) and the predated number of seed per fruits (predated seed per fruit) are also shown. Block was included as a random factor nested on climate change. ms, .0.05 2 ,0.07,
*,0.05; **,0.01, ***,0.001.
3120
control
rain
Figure 3. The effect of climate change (control and rain
levels) and detritivores (Dþ denotes presence (filled circles),
D2 denotes absence (oepn square)) treatments on the abundance of: (a) generalist sapsuckers, and (b) generalist
chewers associated to Moricandia moricandioides. Mean +
s.e. are shown. n¼104 plants.
the plant, indicating that plants compensated for the
reduction in fruit production under the rain level by
an increasing investment on ovules such that more of
them successfully developed into seeds. Short-lived
plants are supposed to be more sensitive to changing
climatic conditions than long-lived plants [24,57];
nevertheless, plants in arid and semiarid areas are
well adapted to annual fluctuation in precipitation
[58]. Indeed, short-lived plants in arid and semiarid
ecosystems respond very rapidly to pulses of precipitation producing large quantities of seeds [59]. This
agrees with the compensatory response of M. moricandioides observed in our study, a plant species in which
most individuals reproduce just once, and only a few
individuals reproduce more than one year (maximum
3 years). Our finding supports the idea that plants
are less affected by changing climatic conditions than
other trophic levels [24,60].
The effect of detritivores on flower and fruit numbers produced by the plants under the rain level was
not unexpected. It is well known that plant responses
to detritivores are variable among plant species [61],
and also vary according to nutrient availability in the
ecosystem [62]. However, our results also indicate
that both factors do not act in isolation and that the
effect of one factor can be reversed by the other. The
mechanism(s) behind the patterns we have observed
are not yet clear. Plants’ resource allocation to
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Climate change and trophic interactions A. González-Megı́as and R. Menéndez
no. of seed predators
8
7
6
5
4
3
*
2
seed predator attack rate
1
0.55
0.50
0.45
0.40
0.35
0.30
0.25
0.20
0.15
0.10
*
control
rain
Figure 4. The effect of climate change (control and rain levels)
and detritivore (Dþ denotes presence (filled circles), D2
denotes absence (open square)) treatments on the number of
seed predators and seed predator attack rate in Moricandia
moricandioides. Mean + s.e. are shown. n ¼ 68 plants.
chemical defence versus reproductive tissue may be
influenced by both climatic conditions and detritivores. We know, from our previous work, that
detritivores in our study system play an important
role in the induction of plant defences (e.g. glucosinolates), in both the vegetative [51] and reproductive
tissues [61]. Several studies have also shown that detritivores affect the production of induced chemical
defences in plants in other systems [63– 65]. These
effects could be due to an increase in nitrogen availability for the plant mediated by detritivores, but
may also be due to detritivores inducing the expression
of genes associated with plant defences [64]. We also
know, from the results presented here, that detritivores
decrease the quality of seeds in the control level, but
increase the seed quality in the rain level (C/N content
of seeds). So we believe that the negative effect of detritivores on flowers and fruits under enhanced rain
may be the result of an increased investment by the
plant into chemical defence and seed number within
fruits, combined with a general higher quality of
those seeds (C/N) in this treatment.
The most intriguing findings of our study are those
related to the effect of the experimental treatments on
the interaction between herbivores and detritivores.
Rainfall alteration had a strong effect on the interaction between detritivores and several above-ground
herbivorous guilds (sapsuckers and chewers), and
those effects also vary with the level of specialization
of the herbivorous guild (generalist versus specialist
herbivores). While other studies have found an effect
of changes in water availability on species interactions
Phil. Trans. R. Soc. B (2012)
3121
(e.g. between above-ground and below-ground herbivores [32,34,66], our results are novel because they
provide empirical evidence that climate change affects
also the interaction between species belonging to
different trophic levels.
The differential response of specialist versus generalist herbivores may be related to the fact that plant
defences are usually more effective against generalist
rather than specialist herbivores [67,68]. The result
that the rain level affected the interaction between detritivores and generalist herbivores could be explained
by a change, due to water availability, in the effect of
detritivores on glucosinolate production by the plant.
In Brassicaceae species, glucosinolate content in different parts of the plant varies under different water
regimes [69,70], and according to the timing of the
irrigation relative to the stage of the plant [71]. In a
resource-limited environment, such as an arid or a
semiarid environment, plant traits that reduce herbivory are important because of the low potential of
plants to compensate for the negative effects of herbivory through growth [72]. Therefore, when nutrient
and/or water levels are insufficient and limit plant
growth, the investment in secondary metabolites
(including plant defence compounds) is low [72].
However, when water and/or resource availability
increases, plants can invest more into defences against
generalist herbivores. Detritivores can also induce
other plant defences against specialist herbivores. We
know, from our previous work on the study system,
that detritivores enhanced parasitoid attack rate of
specialist butterfly species, which seems to indicate
that detritivores are somehow involved in the induction of plant volatile compounds that attract
parasitoids [51] as many plants use induced volatile
metabolites to attract natural enemies as a defence
against specialist herbivores [73,74]. The number of
eggs laid on plants by the specialist butterfly species
was not affected by our experimental treatments,
which suggest that the attraction of parasitoids, or
other types of predator, is required to account for
the negative effect of detritivores on the number of
pierid larvae found on the plants. However, in contrast
to glucosinolates, volatile metabolites may be less
influenced by water availability, as we did not find a
significant interaction effect of detritivores and climate
change on the abundance of specialist herbivores. Crucially, our results support other empirical studies that
have found that generalists and specialists differentially
respond to climate change [10,11]; however, our
results suggest that this differential response of herbivores may be manifested only in the presence of
detritivores within the ecosystem.
Future changes in climatic conditions may have
important implications not only for free-living insects,
but also for endophytic insects. For example, Staley
et al. [34] found that different climatic conditions
altered the competitive interaction between a root herbivore and a leave-miner. In our system, the seed
predator Crossobella trinotella is an endophytic species
that shows a strong association with the fruit during
the complete development of their immature stages.
Our experiment shows that climate change treatment
not only affected the intensity of the interaction
Downloaded from http://rstb.royalsocietypublishing.org/ on June 18, 2017
3122
A. González-Megı́as and R. Menéndez
Climate change and trophic interactions
between detritivores and seed predator abundance, but
also the sign of the interaction from positive (under
current climate conditions) to negative (under a different rainfall scenario). This reversal can be explained by
the low number of flowers produced by the plant
under the rain level, and the negative effect of rain
on the fruit set. Usually, this type of seed predator
lays eggs on flowers, and the larva hatch when the
immature fruits start to develop. In our study, however, the interaction between detritivores and seed
predators was also evident when comparing seed predator attack rate. Therefore, something more than a
reduction in fruit set is required to explain our results.
A possible mechanism behind the pattern detected is
that seed predator attack rate is related to the quality
of the resource. Curiously, although our experiment
shows that in the control level, detritivores decreased
seed quality, with no significant effect of detritivores
treatment in the rain level, seed predator attack rate
was not related to the C/N content in seeds. An
alternative, non-exclusive mechanism to explain our
results is that the effect of rain on the interaction
between detritivores and seed predators may be
mediated by an increase within the seeds of primary
and secondary metabolites produced by the plant.
Detritivores affected the quality of the seeds in our systems by increasing the glucosinolate content of seeds
[75], which could have a positive effect on a specialist
herbivore such as C. trinotella by reducing competition
or accidental predation by generalist herbivores feeding on fruits [67,68].
5. CONCLUDING REMARKS
Ecosystems are expected to experience changes in climatic conditions in the future, which include not only
temperature and UV-radiation changes, but also rainfall alterations. Therefore, to understand and predict
the effects of future climate change on drylands, we
need an improved understanding of how rainfall affects
the abundance of species as well as the sign and
strength of interactions between different components
of above- and below-ground communities inhabiting
those ecosystems [16,19]. This study contributes to
this understanding by focusing on the effect of rainfall
intensity and frequency on tritrophic interactions linking species from the above-ground and below-ground
subsystems. Our results support the idea that different
trophic levels will be differentially affected by climate
change. Rain alteration changed the effect of belowground organisms on plant traits, but with no net
effect on plant reproductive output. In addition, our
rain manipulation affected in a contrasting way the
interaction between organisms belonging to different
trophic levels, and also species with different trophic
specializations. Climate change will not only affect
the strength of species interactions, but, as found in
our study, may also turn positive interactions into
negative ones (or vice versa), leading to disruptions
within the wider food web with potential consequences
for ecosystem functioning [16,19,20]. The complex
responses found in this study suggest that future climate change will affect trophic levels and their
interactions differentially, making extrapolation from
Phil. Trans. R. Soc. B (2012)
individual species’ responses and from one ecosystem
to another very difficult.
We thank Ignacio Villegas, Viola Belohrad and Mara Lindtner
for their help in the lab and in the field, and Mark Lineham
for kindly revising the English in the manuscript. We also
thank three anonymous reviewers for insightful reviews
of this manuscript. We are grateful to J. M. Nieto Nafrı́a
(Aphids), Oscar Aguado (Tenthedinidae), Vladimir
Gnezdilov (Issidae) and Ole Karsholt (Gelechiidae) for the
identification of the specimens. This research was funded
by a grant (P08-RNM-0381) from the Andalusian
Government, Spain.
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