Download Direct effects of elevated temperature on a tri-trophic system

Arthropod-Plant Interactions
DOI 10.1007/s11829-015-9401-0
ORIGINAL PAPER
Direct effects of elevated temperature on a tri-trophic system:
Salix, leaf beetles and predatory bugs
Adriana Puentes1 • Mikaela Torp1 • Martin Weih2 • Christer Björkman1
Received: 20 August 2014 / Accepted: 16 October 2015
Springer Science+Business Media Dordrecht 2015
Abstract The net effect of climatic change on biotic
interactions will depend on how each interacting species is
individually affected. Elevated temperatures are predicted
to have differential effects on species across trophic levels,
due to asymmetric sensitivity to temperature changes. In
this study, we examined the direct effects of three temperature regimes (16, 20 and 24 C) that reflect present
and, potentially, future climate conditions on the response
of Salix spp. plants, an important bioenergy crop, and its
most damaging herbivore (Phratora vulgatissima) and an
efficient natural enemy (the omnivorous predator
Orthotylus marginalis). We found that plant growth, herbivore oviposition and enemy egg-foraging rate correlated
positively with temperature. In the event of elevated temperatures following global climatic changes, these species
could potentially respond in tandem. Still, the strength of
responses varied among species, with herbivore and natural
enemy exhibiting a similar and steeper rate of response
relative to plants. Additionally, the herbivore’s response
was influenced by plant quality with altered oviposition
rates depending on whether it was fed the (previously
determined) resistant Salix dasyclados or susceptible S.
viminalis. This indicates that host plant chemistry has the
potential to mediate differential responses to temperature.
Together, our results suggest that indirect effects of
Handling Editors: Rupesh Kariyat and Heikki Hokkanen.
& Adriana Puentes
[email protected]
1
Department of Ecology, Swedish University of Agricultural
Sciences, Box 7044, 750 07 Uppsala, Sweden
2
Department of Crop Production Ecology, Swedish University
of Agricultural Sciences, Box 7043, 750 07 Uppsala, Sweden
elevated temperatures, leading to a disruption of trophic
associations, may be less likely or less severe in this tritrophic system.
Keywords Climate change Global warming Trophic
interactions Pest Natural enemy
Introduction
A major challenge for both basic and applied ecologists is
to understand and predict how global environmental
change will affect interactions among species. Complex
networks of biotic interactions such as pollination, parasitism and predation play a pivotal role in maintaining
biodiversity and stabilizing key ecosystem services (Bascompte et al. 2006; Ives and Carpenter 2007). Nonetheless,
the effects of large-scale environmental changes on interacting species has only recently received its deserved
attention, and a comprehensive framework has yet to be
fully developed (Bale et al. 2002; Parmesan 2006; Voigt
et al. 2007; Tylianakis et al. 2008; Berggren et al. 2009;
Jamieson et al. 2012; Rosenblatt and Schmitz 2014). In
particular, the effects on interactions involving more than
two trophic levels remain understudied (Jeffs and Lewis
2013; Facey et al. 2014). This is surprising given that
important tri-trophic associations such as the one between
plants, herbivores and enemies can be substantially disrupted, for example, by increases in temperature (Harrington et al. 1999; Hoover and Newman 2004; Barton
et al. 2009; de Sassi and Tylianakis 2012; Gillespie et al.
2012; Dyer et al. 2013). A necessary first step, for a
complete understanding of changes in interaction strength,
is to assess responses to climatic stress at different trophic
levels (Sentis et al. 2013; Butt et al. 2015). To this end, we
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A. Puentes et al.
examined the effects of increased temperature on the performance of species at three trophic levels: two plant
species, Salix spp., a leaf-chewing herbivore, Phratora
vulgatissima and one of its most important enemies, the
omnivorous predator Orthotylus marginalis.
Elevated temperatures are predicted to affect members of
the different trophic levels in different ways, and these
effects can be direct or indirect. Effects directly related to
temperature include, for example, changes in the organism’s
physiology, phenology or behavior. For plants, direct effects
of elevated temperature are usually positive, with an
increase in plant growth and primary productivity (Rustad
et al. 2001; Weih 2001 for Salix), but the effects can be
variable (Smith et al. 2015). Likewise, performance and
survival of insects are expected to be positively affected
through faster developmental rates and increased voltinism
with rising temperatures (Bale et al. 2002; Robinet and
Roques 2010). On the other hand, high temperatures can
have direct negative consequences on the survival of
invertebrate natural enemies, for instance, through longer
parasitoid developmental times (Gillespie et al. 2012) and
higher risk of starvation (Rall et al. 2009). Those natural
enemies with highest specialization would be most at risk,
while others with flexible food preferences, like omnivorous
predators, are expected to be less susceptible (AguilarFenollosa and Jacas 2014). Albeit great variation in
responses at different trophic levels (Tylianakis et al. 2008),
the general trend that emerges is that sensitivity to changes
in temperature, and other climatic variables increases with
trophic level (Voigt et al. 2003, 2007; Berggren et al. 2009;
Jeffs and Lewis 2013; Facey et al. 2014).
Differential sensitivity to temperature across species and
trophic levels is likely to result in members of communities
not responding in tandem to climatic changes. As a consequence, trophic associations may be disrupted and the
indirect effects of temperature will be mediated by
enhancement or weakening of interaction strength (Voigt
et al. 2007; Tylianakis et al. 2008). For example, asynchronous responses to elevated temperatures have been
documented in several plant–herbivore and host–parasitoid
systems, with most studies reporting negative effects on the
strength of interactions (de Sassi and Tylianakis 2012;
Romo and Tylianakis 2013; Dyer et al. 2013; Sentis et al.
2013; but see Klapwijk et al. 2010; Barton 2011). A
weakening of host–parasitoid interactions can result in a
greater potential for insect outbreaks and lower plant biomass (Hoover and Newman 2004; Parmesan 2006; de Sassi
and Tylianakis 2012). Likewise, plant-mediated effects can
also cascade upward; changes in host plant nutritional and
defensive chemistry due to greater temperatures can negatively affect both herbivore and, indirectly, parasitoid
performance (Gillespie et al. 2012; Dyer et al. 2013).
Alteration of plant defense expression, for instance, can
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have important consequences for the food preference of
omnivorous predators and for localization of prey by
means of induced plant volatiles (DeLucia et al. 2012;
Jamieson et al. 2012; Ode et al. 2014). Understanding and
forecasting such temperature-driven disruptions of trophic
interactions is a pressing need (Aguilar-Fenollosa and Jacas
2014), particularly so for agricultural systems already
experiencing a dampening of natural enemy efficiency
(Montserrat et al. 2013). To achieve better forecasting of
ecological changes, direct and indirect responses by individual species need to be quantified and teased apart (Suttle
et al. 2007; Barton et al. 2009; Gilman et al. 2010).
The aim of this study was to examine the individual
responses of species from three different trophic levels to
temperature regimes that reflect present and, potentially,
future climate conditions. We examined the direct effects
of temperature on plant biomass of two Salix species, S.
dasyclados and S. viminalis, on the egg-laying rate of the
leaf-chewing herbivore P. vulgatissima and on the eggconsumption rate of the omnivorous predatory bug O.
marginalis. Due to high biomass production and efficient
nutrient use, varieties of Salix spp. are frequently used in
short rotation forestry for biomass production (Karp and
Shield 2008; Kuzovkina et al. 2008); the two used in this
experiment exhibit contrasting levels of resistance against
the most severe insect pest of these plantations, P. vulgatissima (Lehrman et al. 2012). This beetle can cause
substantial growth losses (Björkman et al. 2000), but
control of this pest’s population growth can be achieved
through its most efficient natural enemy O. marginalis,
which feeds on eggs and larvae of the beetle (Björkman
et al. 2004; Dalin et al. 2011). Based on previous research
on direct effects of temperature on plant physiology and
arthropod metabolism, we expect plant biomass, egg-laying by the herbivore and egg-consumption by the omnivorous predator to increase with temperature. However,
since sensitivity to temperature is expected to positively
correlate with trophic level, the rate of increase should be
lowest for plants and greatest for the omnivorous predator
(cf. Figure 4 in Berggren et al. 2009). That is, the degree of
steepness in responses is hypothesized to follow this order:
plant \ herbivore \ omnivore. Moreover, an increase in
egg-laying by the herbivore should be disrupted by the
level of plant resistance, with herbivores expected to lay
eggs at a slower rate on the more resistant species, S.
dasyclados.
Materials and methods
The response of plants, herbivore and omnivorous predator
to different temperatures (16, 20 and 24 C) was assessed
under laboratory conditions by conducting three separate
Direct effects of elevated temperature on a tri-trophic system: Salix, leaf beetles and…
experiments at the Swedish University of Agricultural
Sciences (SLU), Uppsala, Sweden (59490 N, 17400 E).
Temperatures were selected to reflect present and potentially future climate conditions around mid- to south-central Sweden, where Salix spp. plantations are most
common. The lowest temperature (16 C) corresponds to
the current mean temperature in Uppsala, central Sweden,
during the time of the year when the insect herbivore and
predator are active (May/June, Swedish Meteorological
and Hydrological Institute, SMHI). An increased mean
temperature of 20 C during the summer months for this
area would be a reasonable expectation following climate
change. While, the highest temperature treatment (24 C)
will most likely not be relevant in the near future, but may
be so for other parts of central and southern Europe where
there is an increasing interest in growing Salix spp. as a
bioenergy crop.
area of experimental plants could not be assessed nondestructively, we measured leaf area on and weighed a separate group of control plants at the start of the experiment
(n = 9 per species). These were taken from the same group
of original plants grown in the glasshouse, so they were
reared under same conditions and were of same age
(22 days). Thus, average changes in biomass or leaf area
per species can be reasonably assessed by using the values
after 14 days of treatment and values of these control
plants. Aboveground biomass was collected and oven-dried
(70 C) for 48 h before weighing. Leaf area (cm2) was
determined by scanning five fresh leaves from each plant;
areas were measured using WinDIAS, Delta-T SCAN
(Delta-T Devices Ltd., Cambridge, UK). The length of the
main shoot (cm) was measured for each experimental plant
at the start and after 14 days of treatment; internode length
(cm) was estimated by dividing the length of the main
shoot by the number of internodes.
Plants
Herbivore
To examine plant responses to different temperatures, we
used two different Salix sp. (Salicaceae) varieties, i.e., the
S. dasyclados L. hybrid variety ‘Loden’ and the S. viminalis L. natural variety ‘L78021’ (see Kendall et al. 1996).
Salix dasyclados has been characterized as being much
more resistant to P. vulgatissima, in terms of beetle survival and oviposition, than S. viminalis (Glynn et al. 2004;
Lehrman et al. 2012).
Winter cuttings of the two Salix species were collected
in 2010 from plantations around Uppsala and stored at 4 C
until the experiment was due to start at the beginning of
July. From storage, cuttings were divided into 5-cm pieces,
with each piece containing at least two buds. Ninety of
these cuttings, per species, were planted individually in
plastic pots (height = 10 cm, diameter = 9 cm) filled with
soil (85 % peat, 15 % sand) containing NPK fertilizer
(N = 180, P = 110, K = 195 g/m3). Plants were left to
grow in a glasshouse at 22, 20 C during the day and night,
respectively, and with a 16:8-h (L:D) photoperiod. After
22 days, plants were transferred to different growth
chambers (Percival Scientific Inc., Perry, IA, USA) with
the following settings: 16/16, 20/16 and 24/16 C day/night
with a 16:8-h (L:D) photoperiod, RH: 75 %, and a light
intensity of 300 lm. Night temperatures were not manipulated due to technical difficulties. Plants were randomly
assigned to one of the three temperature treatments
(n = 18 per species 9 treat combination) and to the two
shelves of each growth chamber; they were rotated
between shelves daily.
We examined the effects of temperature on total
aboveground biomass, leaf area, and shoot and average
internode lengths. Plants were harvested after 14 days of
treatment. Since the starting aboveground biomass or leaf
To examine herbivore responses to different temperatures,
we used females of the leaf-chewing beetle Phratora vulgatissima L. (Coleoptera: Chrysomelidae). Phratora vulgatissima causes severe damage to Salix spp. plants and in
plantations larval and adult feeding can result in growth
losses of up to 40 % (Björkman et al. 2000). The beetle
overwinters as an adult, and it is univoltine. In Sweden, it
aggregates on preferred host plants in early May and after a
short period of feeding, mates and lays eggs until mid-late
June. Females lay several clutches of 5–50 eggs (even up to
[500 eggs in total) on the underside of leaves at the base
of shoots; eggs hatch after 15–20 days (Kendall et al.
1996). After passing through three instar stages, each with
increasing mobility, the larvae pupate in the soil.
In February and March 2010, overwintering Phratora
vulgatissima beetles were collected from natural stands of
Salix cinerea around Uppsala. Beetles were stored at -5 C
to avoid disruption of their hibernation period. Three weeks
before the start of the experiment (beginning of July), they
were transferred to ambient room temperature. During this
period, males and females were placed together in cages
containing either S. dasyclados or S. viminalis and allowed
to mate. At the start of the experiment, females were separated from males and transferred individually to plastic
containers (height = 7 cm, diameter = 3 cm) with perforated screw caps. They were fed detached, fully developed
leaves kept on a piece of well-watered oasis foam in the
container. Leaves originated from S. dasyclados or S.
viminalis plants that had been grown in a glasshouse for
about 2 months. Female beetles (one per container, n = 20
per plant species they were reared on) were placed in
growth chambers at 16, 20 or 24 C with the same settings
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as the plant experiment described above. Every second day,
they were provided with fresh leaves, and the number of
eggs laid were counted and removed from the container.
The experiment lasted for 14 days and beetles that died
during this period were excluded from statistical analyses.
Omnivorous predator
To examine predator responses to different temperatures,
we used nymphs of the omnivorous predator Orthotylus
marginalis Reuter (Hemiptera: Miridae). Orthotylus marginalis is the most abundant and effective natural enemy of
P. vulgatissima in Salix spp. plantations (Björkman et al.
2003, 2004). In Sweden, it has one generation per year and
overwintering occurs as eggs with nymphs appearing in
early May; adults are present until late August. Orthotylus
marginalis is a generalist predator, feeding on aphids and
mites as well as P. vulgatissima, and when needed it
obtains fluids from leaves and fruits of several deciduous
trees including Salix spp. (Wheeler 2001).
Nymphs of O. marginalis were collected from natural S.
cinerea stands located around Uppsala in 2010. They were
placed in a refrigerator and not allowed to feed for 24 h
prior to start of the experiment (beginning of July). Phratora vulgatissima eggs were obtained from beetles that
previously fed and laid eggs on S. viminalis leaves. For the
experiment, 10-cm-long shoots of S. viminalis were placed
in water in plastic containers and covered with perforated
plastic bags that are large enough to allow insect movement. Leaves or parts of leaves holding P. vulgatissima
eggs were pinned to the covered S. viminalis shoots. Each
shoot received one clutch of eggs and although there was
variation, there were enough eggs to feed O. marginalis
during the experimental period. One nymph was placed on
each of the S. viminalis shoots (n = 40 per temperature
treatment) and transferred to growth chambers at 16, 20 or
24 C with the same settings as the plant experiment
described above. Nymphs were allowed to feed for 24 or
48 h, depending on the egg clutch size, and the number of
eggs consumed was determined after this period.
Dead/parasitized nymphs were excluded from the statistical analyses. Due to logistical limitations and availability
of O. marginalis, it was not possible to examine effects of
temperature on the consumption of eggs reared on S.
dasyclados.
Data analyses
In order to examine the effects of temperature on plant,
herbivore and omnivore responses, we fitted several linear
models. All analyses were conducted in R (version 3.1.2, R
Development Core Team 2015). For plant responses,
changes in aboveground biomass, area per leaf, shoot and
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average internode lengths between the start and end of the
experiment were first calculated. Separate models were
fitted for each response variable, which included temperature (three treatments: 16, 20 and 24 C), species (two
species: S. dasyclados and S. viminalis) and their interaction as explanatory variables. Herbivore and omnivore
responses were calculated as egg-laying and egg-consumption rates per day, respectively. Models to examine
effects on egg-laying included the same explanatory variables as models examining plant responses (temperature
and species), while models to examine egg-consumption
only included temperature (S. dasyclados was not used, see
‘‘Materials and methods’’ Section). Analysis of variance
(ANOVA) was used to test the significance of main effects
and interactions. Data were checked for homogeneity of
variance and normality; the herbivore response variable,
egg-laying rate, required square-root transformation to
meet these assumptions.
Results
Plants
Temperature had a significant and positive effect on plant
growth, but the strength of responses varied among the two
Salix species (Table 1; Fig. 1c). Changes in aboveground
biomass (Fig. 1c) and in shoot length were more pronounced
for S. viminalis [mean (cm) ± S.E.; 16 C = 7.53 ± 0.40,
20 C = 9.06 ± 0.38, 24 C = 19.62 ± 0.60] than for S.
dasyclados [mean (cm) ± S.E.; 16 C = 3.77 ± 0.62,
20 C = 4.60 ± 0.77, 24 C = 9.42 ± 1.45]. On the other
hand, leaf area [mean (cm2) ± S.E.; S. viminalis:
16 C = 3.71 ± 0.68, 20 C = 4.44 ± 0.84, 24 C =
11.02 ± 2.04; S. dasyclados: 16 C = 1.40 ± 0.68,
20 C = 2.78 ± 0.97, 24 C = 5.65 ± 2.26] and average
internode length [mean (cm) ± S.E.; S. viminalis: 16 C =
0.08 ± 0.02, 20 C = 0.05 ± 0.01, 24 C = 0.18 ± 0.03;
S. dasyclados: 16 C = 0.12 ± 0.03, 20 C = 0.15 ± 0.03,
24 C = 0.28 ± 0.04] also increased with temperature, but
responses were not statistically different (i.e., no significant
treatment 9 species interactions; Table 1) between the two
plant species. Changes in biomass and leaf area were
assessed using values that were separately calculated in a
control group of plants [see ‘‘Materials and methods’’ Section for details; mean biomass control (g): S. viminalis = 0.073, S. dasyclados = 0.032; mean leaf area
control (cm2): S. viminalis = 3.05, S. dasyclados = 0.96].
Herbivore and omnivorous predator
Temperature had an overall positive effect on egg-laying
and egg-consumption by P. vulgatissima and O.
Direct effects of elevated temperature on a tri-trophic system: Salix, leaf beetles and…
Table 1 Results from a two- or
one-way analysis of variance on
the effects of temperature (16,
20 or 24 C), species (S.
viminalis and S. dasyclados) and
their interaction on
aboveground production (g),
changes in leaf area (cm2), shoot
and average internode length
(cm) of plants, and on the egglaying and egg-consumption
rates of the herbivore P.
vulgatissima and omnivorous
predator O. marginalis (only
tested on S. dasyclados)
Response variable/source of variation
d.f.
MS
F
P
Aboveground production
Temperature
2
0.75
16.85
\0.0001
Species
1
3.45
77.94
\0.0001
Temperature 9 species
2
0.17
3.80
0.029
48
0.04
Temperature
2
168.87
10.68
0.0002
Species
1
130.38
8.24
0.0061
Temperature 9 species
2
17.41
1.10
0.341
47
15.82
Error
Leaf area
Error
Shoot length
Temperature
2
835.90
78.95
\0.0001
Species
1
1021.80
96.50
\0.0001
Temperature 9 species
2
112.10
10.58
\0.0001
102
10.60
Temperature
2
0.22
15.39
\0.0001
Species
1
0.16
11.41
0.001
Temperature 9 species
2
0.01
0.79
0.459
102
0.01
Error
Internode length
Error
Eggs laid/day
Temperature
2
5.64
25.58
\0.0001
Species
1
77.06
349.63
\0.0001
Temperature 9 species
2
0.75
3.39
0.038
89
0.22
2
204.00
7.21
0.0027
31
28.30
Error
Eggs consumed/day
Temperature
Error
Significant effects (P \ 0.05) are in bold
marginalis, respectively (Table 1; Fig. 1a, b). In both
cases, but particularly so for the herbivore, the increase in
egg-laying and consumption was greatest and most pronounced between 16 and 20 C compared with that
between 20 and 24 C (Fig. 1a, b). Moreover, the temperature effect on egg-laying varied between plant species
(Table 1). Leaf beetle females that were previously fed and
allowed to oviposit on S. dasyclados laid fewer eggs
compared with those on S. viminalis (Fig. 1b).
Comparison of responses among trophic levels
Overall, the relative response of the plant (S. viminalis), the
herbivore and omnivorous predator to the temperature
regimes was similar; an increase in temperature was followed
by an increase in response variables (Fig. 2a). However, the
rate of increase differed across trophic levels, especially when
comparing the plant’s response to that of the herbivore and
omnivore. The greatest relative response was observed at
24 C for S. viminalis (Fig. 2a). On the other hand, when
examining responses of and on S. dasyclados, the plant and
herbivore had an extremely similar pattern in their relative rate
of increase across temperature regimes (Fig. 2b).
Discussion
Our study examining the direct effects of different temperature regimes on species at three trophic levels showed
that the growth, oviposition and foraging responses of
plants (Salix spp.), herbivore (P. vulgatissima) and
omnivorous predator (O. marginalis), respectively, correlated positively with temperature. Hence, in the event of
elevated temperatures following global climatic changes,
these species could potentially respond in tandem.
Nonetheless, the strength of responses varied among species, and in particular, the herbivore’s rate of response was
influenced by host plant quality.
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A. Puentes et al.
OMNIVOROUS PREDATOR
eggs consumed day −1
25
Direct effects of temperature
(a)
In line with previous studies, elevated temperature directly
affected plant growth, herbivore oviposition rate and
predator foraging rate. Both plant species, S. viminalis and
S. dasyclados, exhibited an increase in plant biomass at
greater temperature (Fig. 1c). Warmer temperatures tend to
accelerate plant growth, for example, by increasing net
photosynthesis or extending the growing season (Rustad
et al. 2001; Weih 2001 for Salix; Norby and Luo 2004;
Jamieson et al. 2012). Nonetheless, responses can be
variable among plant species and vegetation types (Wu
et al. 2011; Smith et al. 2015). Likewise, temperature is
known to affect the rate of metabolic processes in insects
(Irlich et al. 2009). In our experiment, we found that both
the herbivore P. vulgatissima and omnivorous predator O.
marginalis increased their egg-laying and egg-consumption
20
15
10
5
0
18
(b)
16
HERBIVORE
eggs laid day −1
14
2.5
10
Salix viminalis
2.0
8
1.5
6
Relative temperature response
4
2
0
1.4
Salix viminalis
Salix dasyclados
(c)
1.2
PLANT
aboveground production (g)
(a)
12
1.0
Omnivore
Herbivore
Plant
1.0
0.5
2.5
(b)
Salix dasyclados
2.0
0.8
1.5
0.6
1.0
0.4
0.5
0.2
0.0
16 °C
16 °C
20 °C
24 °C
Fig. 1 Effects of the three temperature regimes (16, 20 and 24 C) on
(a) consumption rate (mean number of eggs consumed/day ± S.E.) of
the omnivorous predator Orthotylus marginalis, b oviposition rate
(mean number of eggs laid/day ± S.E.) of the herbivore Phratora
vulgatissima reared on either Salix viminalis or S. dasyclados and
c aboveground production [mean change in biomass (g) ± S.E.] of S.
viminalis or S. dasyclados following 14 days of treatment
123
20 °C
24 °C
Temperature
Fig. 2 Relative responses to three different temperature regimes (16,
20 and 24 C) of (a) the herbivore-susceptible Salix viminalis, the
herbivore Phratora vulgatissima and omnivorous predator Orthotylus
marginalis reared on S. viminalis, and of the (b) herbivore-resistant S.
dasyclados and the herbivore P. vulgatissima reared on S. dasyclados.
Aboveground production, egg-laying and consumption were relativized using the values of these variables at 16 C
Direct effects of elevated temperature on a tri-trophic system: Salix, leaf beetles and…
rates, respectively, at greater temperatures (Fig. 1a, b).
This is in agreement with previous experiments showing
that temperature can positively influence herbivore fecundity (Bale et al. 2002; Cornelissen 2011) and egg-consumption in some arthropod predators (Parajulee et al.
2006).
Comparison of responses among trophic levels
Plants, herbivore and omnivorous predator responded in
tandem to increasing temperature in our experiment, but
differential responses across trophic levels may occur more
often than not (Voigt et al. 2003; Tylianakis et al. 2008;
Laws and Joern 2015). For instance, in studies examining
responses of plants, herbivores and natural enemies, temperature can have a small positive effect on plants, disproportionately benefit herbivores, and negatively affect
parasitoids (de Sassi and Tylianakis 2012; Dyer et al.
2013). On the other hand, there can be no change in plant
biomass, and a negative effect on both herbivore and
predator performance following elevated temperatures
(Gillespie et al. 2012; Sentis et al. 2013). These differential
responses to temperature are thought to be due to asymmetric sensitivity to temperature across trophic levels
(Berggren et al. 2009). While plants, herbivore and
omnivorous predator did respond similarly in our experiment, the strength of responses varied among them. We
expected the strongest (i.e., steepest) and weakest response
to occur for the predator and plant, respectively. The pattern of relative responses on S. viminalis lends partial
support to this expectation (Fig. 2). When exposed to an
elevated temperature of 20 C, plants do exhibit a weaker
(i.e., less steep) response than herbivores and omnivores
(Fig. 2a). Given that plants should be the least sensitive, a
greater change in temperature would be required to observe
a response (Berggren et al. 2009); the observed steeper
increase in plant biomass at 24 C would be in line with
this idea (Fig. 2a).
On the other hand, the omnivorous predator O. marginalis did not exhibit the strongest response to temperature; in fact, the response was similar to that of the
herbivore P. vulgatissima (Fig. 2a). Because predators are
generally more active foragers and should have higher
metabolic rates than herbivores, they are expected to show
a stronger response to temperature (Voigt et al. 2003).
However, O. marginalis has been described as a ‘find-andstay’ predator (Björkman et al. 2003) and could be less
active relative to other arthropod predators and specialized
natural enemies like parasitoids, on which many of the
temperature-related expectations are based. Moreover, O.
marginalis can use plants as a food source, and this is
expected to provide some buffer in responses to climatic
changes (Aguilar-Fenollosa and Jacas 2014). Thus, given
the special characteristic of O. marginalis, similar strength
of response among herbivore and natural enemy (relative to
the plant) may not be unreasonable in this tri-trophic
system.
Together, our results suggest that if plant, herbivore and
predator respond uniformly to changes in temperature, a
disruption of trophic relationships is less likely or less
pronounced (Voigt et al. 2003; Tylianakis et al. 2008). For
example, if temperature-driven direct responses are similar,
negative indirect effects such as asynchrony between herbivore and natural enemy may not occur or be less severe
(Aguilar-Fenollosa and Jacas 2014). This is of particular
relevance for the biocontrol of P. vulgatissima, which can
reach outbreak densities in Salix spp. plantations and shows
variation in the ability to adjust oviposition rate to temperature (Björkman et al. 2011). While temperature may
not or to a lesser extent alter the relationship between P.
vulgatissima and O. marginalis, other climatic variables
are also likely to change along with temperature and could
disrupt their interaction. As species interactions are context
dependent, insect responses to a climatic variable in isolation can differ from those responses to multiple variables
changing simultaneously (Rosenblatt and Schmitz 2014).
Effects of host plant quality on herbivore
performance
We found that the herbivore, P. vulgatissima, was sensitive
to the level of host plant resistance it was reared on, and its
oviposition rate was altered depending on whether it was
fed the resistant S. dasyclados or the susceptible S. viminalis (Fig. 1b). These two plant species differ in their
defensive chemical profiles, and it is not uncommon that
host plant chemistry predicts herbivore performance (e.g.,
Awmack and Leather 2002; Zvereva and Kozlov 2006;
Carmona et al. 2011; Alba et al. 2014). Genotypes of S.
viminalis exhibit high concentrations of condensed tannins
and no salicylates, while S. dasyclados produces salicylates
but lower concentrations of tannins (Lehrman et al. 2012).
In line with our expectations and previous assays, P. vulgatissima laid fewer eggs on S. dasyclados and the
response to temperature was affected (Fig. 2a, b). Surprisingly, the interactive effects of host plant (nutritional
and chemical) quality and climatic changes on herbivore
performance have been little explored, and thus, general
predictions are not straightforward (Zvereva and Kozlov
2006; Cornelissen 2011; Jamieson et al. 2012). For herbivores, the energetic costs of metabolizing plant defense
compounds likely differ depending on host plant chemistry.
In turn, this can affect resources available for other temperature-sensitive biological functions, such as growth and
reproduction (Jamieson et al. 2012). While our experiment
does not allow us to establish a direct association between
123
A. Puentes et al.
defense compounds, temperature and herbivore, it suggests
that host plant chemistry does have the potential to mediate
differential responses to temperature.
Conclusions
We found that the response of species across three trophic
levels, Salix sp., P. vulgatissima and O. marginalis, to
elevated temperature was in the same general positive
direction, but the strength of responses varied. These
results suggest that indirect temperature effects, leading to
a disruption of trophic associations, may be less likely or
less severe in this system. However, we did not simultaneously examine all of the species’ responses to increased
temperature, which limits our ability to make predictions
on consequences for the strength of interactions. In addition, we found that host plant quality altered the oviposition response of the herbivore to the temperature changes.
Previous studies have shown that insect body size can
affect measures of metabolic activity, such as egg output
(e.g., Honěk 1993; Calvo and Molina 2005). Female beetles were kept and fed under same conditions, which should
minimize environmentally driven differences, but we are
not able to determine if body size explains any of the
variation in egg output. Nonetheless, our study is an
important contribution to understanding the direct effects
of environmental change on physiology and behavior at
different trophic levels, which strongly influences interaction strength and community-level responses (Tylianakis
et al. 2008; Gillespie et al. 2012; Aguilar-Fenollosa and
Jacas 2014).
Acknowledgments We thank Karin Eklund and Hans Johansson for
practical help, Mikael Andersson for valuable discussions about
statistics, and Richard Hopkins for editing earlier versions of the
manuscript. CB and MW acknowledge financial support from the
Swedish Energy Agency and the Faculty of Natural Resources and
Agricultural Sciences at SLU (SAMBA-project), the MISTRA-funded project ‘‘Future Forests’’ and the Lamm Foundation.
Compliance with ethical standards
Conflict of interest
of interest.
The authors declare that they have no conflict
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