Agricultural and Forest Entomology (2014), 16, 417–425
DOI: 10.1111/afe.12071
Phenotypic plasticity in host plant preference of the willow leaf
beetle Phratora vulgatissima: the impact of experience made
by adults
Nadine Austel∗ , Christer Björkman† , Monika Hilker∗ and Torsten Meiners1∗
∗ Applied Zoology/Animal Ecology, Dahlem Centre of Plant Sciences, Freie Universität Berlin, Haderslebener Strasse 9, D-12163 Berlin, Germany
and † Department of Ecology, Swedish University of Agricultural Sciences, Box 7044, 750 07 Uppsala, Sweden
Abstract
1 Knowledge of the plasticity of Phratora vulgatissima (Colepotera: Chrysomelidae)
behavioural responses to cues of its willow host plants is essential for understanding
host affiliations of this species and for developing management strategies.
2 We investigated how the experience obtained by adult P. vulgatissima with two
different willow species shapes olfactory, feeding and oviposition preferences in the
laboratory. The willow species differed in their leaf odours and phenolic glycoside
contents.
3 Females that had experienced Salix viminalis (Salicaceae) neither discriminated
between odours of S. viminalis and Salix dasyclados, nor between blends of green
leaf volatiles (GLV) that mimic quantitatively those released by S. viminalis and S.
dasyclados. However, when females had experienced S. dasyclados, they preferred
the experienced odour of S. dasyclados and the respective GLV blend to the odour of
S. viminalis or its GLV blend.
4 By contrast, regardless of their experience obtained in the adult stage, females
preferred S. viminalis over S. dasyclados for feeding and oviposition.
5 Exposure of beetles to odour of stands with various willow species might affect the
experience-induced olfactory preference for a single species and thus impair host
location success.
Keywords Adult experience, Chrysomelidae, feeding, olfaction, oviposition, phenotypic plasticity, Phratora vulgatissima, plant location, Salicaceae.
Introduction
Knowledge of the host plant fidelity of herbivorous pest insects
can help to improve pest management practices and biological
control methods. A crucial prerequisite for host plant fidelity
of herbivorous insects is that they can successfully locate their
plants and assess the suitability of a plant for feeding and
oviposition. Many herbivorous insects locate their host plants by
visual and olfactory cues from a distance (Bernays & Chapman,
1994; Bruce & Pickett, 2011; Beyaert & Hilker, 2014). Upon
contact, they may exploit further physical and chemical contact
cues that provide information on the suitability of the plant for
oviposition and feeding (Courtney & Kibota, 1990; Fernandez
& Hilker, 2007). The variability in preferences of specialized
Correspondence: Torsten Meiners. Tel.: +49 30 83855910; fax: +49
30 83853897; e-mail: [email protected]
1 Present address: Helmholtz-Centre for Infection Research, Inhoffenstraße 7, 38124 Braunschweig, Germany.
© 2014 The Royal Entomological Society
herbivorous insects for host plant species reflects the insect’s
adaptive ability to cope with the variability of host plant traits.
This plant preference plasticity of herbivorous insects may
provide the chance to broaden the host range by colonizing new
plant species with traits similar to those of the current host plant
species or with traits to which the insect is pre-adapted (Ehrlich
& Raven, 1964).
The range of host plants chosen by herbivorous insects is
determined by both the genetic and phenotypic plasticity of the
herbivore (Courtney et al., 1989; Futuyma & McCafferty, 1990;
Jaenike, 1990). Phenotypic plasticity in host plant preference
behaviour of herbivorous insects is the result of a wide range
of factors, such as age (Devaud et al., 2003), the immune state
(Mallon et al., 2003; Peng & Wang, 2009), mating status (Anton
et al., 2007), hunger (Thiery & Visser, 1995; Koschier et al.,
2000; Davidson et al., 2006) or prior experience with host plant
species (Dethier, 1982; Prokopy & Lewis, 1993).
The impact of experience on host plant preferences of insects
has received special attention for a long time. Induced host plant
418
N. Austel et al.
preferences may be mediated by larval (‘Hopkins host selection principle’), pupal and/or early adult (‘neo-Hopkins host
selection principle’ and ‘chemical legacy hypothesis’) experience with plant cues (Hopkins, 1917; Smith & Cornell, 1979;
Jaenike, 1983; Corbet, 1985; Barron, 2001; Schoonhoven et al.,
2005b; Anderson et al., 2013). Furthermore, host plant choice
by herbivorous insects that disperse from their natal habitat can
be affected by stimuli experienced in the natal habitat, a phenomenon that is known as the natal preference induction phenomenon (Davis & Stamps, 2004; Davis, 2008). The experiences
made by insects may either be associated with a positive stimulus
(associative learning) or with cues affecting the insect negatively
(aversion learning); however, also without exposure to associated conditioning stimuli, exposure to plant cues can affect host
plant choices positively (sensitization) or negatively (habituation) (Menzel & Müller, 1996). Experience-mediated host plant
preferences of insects are usually expressed as olfactory preferences mediated by volatile plant cues (Cunningham et al., 1998;
Harari & Landolt, 1999; Radžiutė & Būda, 2012) or feeding
(Saxena & Schoonhoven, 1982; Bernays & Weiss, 1996; Santana
& Zucoloto, 2011) and oviposition preferences mediated especially by contact/taste cues (Prokopy et al., 1982; Cunningham
et al., 1998; Liu et al., 2005; Coyle et al., 2011).
Knowledge of the induction of host plant preferences can
help improve the biological control of herbivorous pest insects
(Walter, 2003; Liu et al., 2005; Schoonhoven et al., 2005c;
Szendrei & Rodriguez-Saona, 2010). Pest management practices
and biological control methods can benefit from distinguishing
between different experience-induced phenotypes of a pest insect
species. Wrong assumptions about behavioural, physiological
or morphological features of the insect population in focus
can have costly consequences for the application of biocontrol
strategies (Diehl & Bush, 1984). Thus, the success of biocontrol
approaches that are based on the manipulation of pest insect
behaviour by plant volatiles depends on the degree of behavioural
plasticity of the targeted insect species (Jallow et al., 2004;
Åhman et al., 2010). The less variable the host plant preferences
of herbivorous insects, the more effective and robust is the
implementation of measures for integrated pest management.
In the present study, we investigated the impact of previous
experience of adult Phratora vulgatissima (L.) (Coleoptera:
Chrysomelidae) with different host plant species on the host
plant preferences of this herbivore. We focused on the impact
of the previous experience that adult beetles made with different
host plant species by feeding upon them. The present study
addressed the impact of this experience on the olfactory, feeding
and oviposition preferences of the beetles for these plants.
The blue willow leaf beetle P. vulgatissima is a main defoliator in willow short rotation coppice (Sage & Tucker, 1998)
and occurs in high population densities (Peacock et al., 1999);
the beetle may cause 25–75% defoliation of willows (Sage &
Tucker, 1997), resulting in significantly reduced wood production (Larsson, 1983; Bach, 1994; Kendall & Wiltshire, 1998;
Björkman et al., 2000). In spring, P. vulgatissima aggregates on
willow trees (Kendall & Wiltshire, 1998; Peacock et al., 1999;
Karp & Peacock, 2004).
Several studies have shown that P. vulgatissmia prefers willows
with low levels of phenolic glycosides, such as Salix viminalis
(L.) (Malpighiales: Salicaceae) over species with high levels
of phenolic glycosides, such as Salix dasyclados (Wimm.),
including (i) field studies determining beetle abundance on
different willow species (Sage & Tucker, 1998; Stenberg et al.,
2010); (ii) laboratory studies investigating feeding preferences
by offering leaf discs of different willow species (Kendall et al.,
1996; Peacock et al., 2003); and (iii) laboratory studies investigating oviposition preferences by exposing beetles to whole
leaves (Stenberg et al., 2010; Lehrman et al., 2012; Torp et al.,
2013). Furthermore, P. vulgatissima has been shown to perform
better on plants with low concentrations of phenolic glycosides
(especially salicylates) than on those with high levels of these
secondary compounds (Kelly & Curry, 1991; Peacock et al.,
2004; Stenberg et al., 2010; Lehrman et al., 2012; Torp et al.,
2013). Nevertheless, a study by Peacock et al. (2001) showed
that P. vulgatissima preferred leaf discs from S. dasyclados
(with a high content of phenolic glycosides; Julkunen-Titto,
1989) in a multiple-choice feeding assay over leaf discs from
10 other willow species, including S. viminalis. These beetles
were sampled in the field from S. dasyclados plants. All of these
studies suggest that the beetle’s host plant feeding preference
is variable; this variability might be a result of either genetic
variation or (experience-mediated) phenotypic plasticity.
When adult P. vulgatissima leave their hibernation sites, they
need to locate their host plants from a distance because hibernation often takes place apart from willow stands (Björkman
& Eklund, 2006). Orientation of adult P. vulgatissima to their
host plants is known to be mediated by visual cues (Björkman &
Eklund, 2006) and olfaction (Peacock et al., 2001). Electrophysiological studies have demonstrated antennal responses of both
sexes to the host plant volatiles (Z)-3-hexenol, (Z)-3-hexenyl
acetate, (E/Z)-𝛽-ocimene and 𝛽-caryophyllene; female adults
additionally show antennal electrophysiological responses to
R-(+)-limonene (Fernandez et al., 2007). Willow species differ in their volatile pattern, and one of the main differences
between the volatile pattern of S. viminalis and S. dasyclados is
the ratio between the green leaf volatiles (GLVs) (Z)-3-hexenol
and (Z)-3-hexenyl acetate (1 : 1 for S. viminalis and 1 : 3 for S.
dasyclados) (Peacock et al., 2001; Fernandez et al., 2007).
To date, no study has addressed whether prior experience with a
host affects olfactory preference for the experienced plant species
or feeding and oviposition preferences of P. vulgatissima. Hence,
in the present study, we conducted laboratory experiments
with P. vulgatissima maintained either on S. dasyclados or
on S. viminalis during their pupal and adult stages. In detail,
we investigated whether: (i) adult P. vulgatissima discriminate
between odours from S. viminalis and S. dasyclados depending
on their prior host plant experience; (ii) experience-dependent
olfactory preference for a host plant is caused by preference
for a host plant specific blend of GLVs; and (iii) feeding
and oviposition preferences are shaped by prior host plant
experience.
Materials and methods
Plants and animals
We collected plant cuttings (20 cm) of S. viminalis (clone
78183) and S. dasyclados (clone Loden) in the surroundings of
Uppsala, Sweden. These cuttings were used for further plant
© 2014 The Royal Entomological Society, Agricultural and Forest Entomology, 16, 417–425
Phenotypic plasticity in host plant preference
propagation in the laboratory. Cuttings were incubated in water
for 2 weeks to induce rooting. Before incubation, they were
submerged once in pyrethroid insecticide for 1 min (Spruzid,
Germany). Cuttings with roots were potted in standardized soil
and grown to at least 60 cm height before offering them to the
beetles for feeding. After defoliation, the plant material was
used for further plant propagations. Plants grew in a climate
chamber under an LD 16 : 8 photocycle at 20 ∘ C and 70% relative
humidity (RH) (200–400 μmol/m2 /s photosynthetically active
radiation; 350–1100 nm mercury vapour lamps; Eye Clean-Ace,
Typ MT400/DL/BH; Iwasaki Electric, Japan).
Adults of P. vulgatissima were collected in early spring 2009
at hibernation sites in the surroundings of Uppsala, Sweden
(59∘ 51′ N, 17∘ 37′ E), near a S. viminalis monoculture plantation.
Beetles were reared on S. viminalis plants in the laboratory
in Berlin, Germany, in wooden cages (30 × 30 × 70 cm3 ) with
gauze walls under the same abiotic conditions as those used for
plant growth (see above). The rearing of P. vulgatissima was
established exclusively on S. viminalis. Preliminary rearing trials
revealed that larvae fed with S. dasyclados showed considerably
reduced performance compared with larvae on S. viminalis. To
use beetles with comparable fitness for the bioassays with adults,
we decided to rear P. vulgatissima exclusively on S. viminalis
during the larval phase and to allow them to experience either
S. viminalis or S. dasyclados only in the adult stage. Because
no artificial diet is known for P. vulgatissima, it was impossible
to obtain naïve adults that had never experienced either of the
willow species in their larval stages.
Conditioning of the beetles prior to the bioassays
To investigate the influence of prior experience with a host
plant species on the behavioural preferences of the beetle,
approximately 100 pupae of the P. vulgatissima culture on S.
viminalis were placed in a wooden cage (30 × 30 × 70 cm3 ) on S.
dasyclados (D-beetles). Another group of pupae (approximately
100) was maintained on S. viminalis (V-beetles). Beetles were
supplied with leaves of potted plants of either host plant species
ad libitum. Only females were used for bioassays because their
host plant choice and egg deposition determines the plant species
where the offspring generation will start feeding. Females that
were used for bioassays were approximately 4 weeks old, mated
and started to oviposit at that time.
Prior to testing the olfactory preference, females were starved
for 24 h in a Petri dish lined with moist filter paper (diameter
9 cm; Rotilabo; Roth, Germany). Beetles that were used for the
feeding and oviposition bioassays were taken out of their rearing
cages and used without any prior starvation period.
Abiotic conditions during bioassays
The olfactometer bioassays were conducted at 21–22 ∘ C and
30–40% RH; the olfactometer set-up was illuminated by defused
light (60 W; Concentra® spot R80 Naturata; Osram, Germany), centrally located above the olfactometer. The feeding and oviposition bioassays were conducted in a climate
chamber under an LD 16 : 8 h photocycle at 20 ∘ C and 70%
RH (200–400 μmol/m2 /s photosynthetically active radiation;
419
350–1100 nm mercury vapour lamps; Eye Clean-Ace, Typ
MT400/DL/BH).
Olfactory preference assay: beetle responses to plant
odours
We tested whether female V-beetles and D-beetles discriminate
between leaf odours from S. viminalis and S. dasyclados by using
a static four chamber-olfactometer (Steidle & Schöller, 1997).
The olfactometer (height 4 cm, diameter 20 cm) was made
of an acrylic glass cylinder with four equally sized chambers
(cylinder segments) separated by vertical plates. The chambers
contained the odour sources and provided four odour fields above
the cylinder where a circular walking area was located (height
1 cm, diameter 20 cm) and where beetles could walk around
and orientate between the odour fields. The walking area was
made of gauze (mesh 0.05 cm) and was closed by a glass plate
(29.5 × 29.5 cm2 ).
One of the chambers of the olfactometer was supplied with cut
leaves of S. viminalis, the opposing chamber was supplied with
leaves of S. dasyclados, and the two adjacent chambers separating the test chambers supplied with leaves were left empty. To
standardize the leaf area for volatile emission, three leaves of S.
viminalis and one leaf of S. dasyclados, which has larger and
wider leaves, were used. Mature leaves (randomly chosen from
the upper third of the plant) were cut from undamaged plants, and
the leaf stalk was immediately sealed by Parafilm® (Pechiney
Plastic Packaging Company, Chicago, Illinois). To control for
any position-biased responses of the beetles, the whole set-up
was rotated at 90∘ after each tested beetle.
We recorded the time spent by the beetles in each odour
field for a period of 5 min and used the observer, version 3.0
(Noldus Information Technology BV, The Netherlands) for data
recording. In total, 22 V-beetles and 25 D-beetles beetles were
tested within 4 days. The leaf material that was offered as odour
source was replaced by fresh material after 1 h of testing (i.e.
after testing a maximum of five beetles with this plant sample).
In total, six or seven plant samples per treatment were tested.
After three beetles, the walking area, and after five beetles, the
whole olfactometer was washed with ethanol and distilled water
and dried with tissue paper.
Olfactory preference assay: beetle responses to GLVs
To determine whether preference for the odour of a host plant
species is a result of plant-specific GLV emissions, we used the
same static four-chamber olfactometer as that described above
but tested the olfactory response of beetles to synthetic GLV
blends mimicking those of S. viminalis and S. dasyclados. The
GLV emissions of S. viminalis and S. dasyclados differ with
respect to the ratio of (Z)-3-hexenol and (Z)-3-hexenyl acetate
(1 : 1 for S. viminalis and 1 : 3 for S. dasyclados) (Peacock
et al., 2001). We mixed these GLVs in ratios of 1 : 1 to mimic
the GLV emission of S. viminalis and 1 : 3 to mimic the GLV
emission of S. dasyclados. The compounds were purchased
from Aldrich (St Louis, Missouri) (purity ≥ 98.0%). Each GLV
blend was diluted in dichloromethane (purity ≥ 95.9%; Roth).
The concentration of each blend was 0.7 μg total GLV/μL
© 2014 The Royal Entomological Society, Agricultural and Forest Entomology, 16, 417–425
420
N. Austel et al.
dichloromethane. A volume of 10 μL of this solution was applied
on a filter paper (Roth; diameter 5.5 cm) (i.e. approximately
7 μg of GLV was applied onto a filter paper). This amount of
GLVs has been shown to elicit significant electroantennogram
responses in P. vulgatissima (Fernandez et al., 2007). After 30 s
of evaporation, the filter paper was placed into a chamber of
the static olfactometer. Dual-choice bioassays were conducted
by placing the GLV blends of S. viminalis and S. dasyclados
in opposite fields; the remaining control fields were supplied
with air only. Twenty-five V-beetles and 28 D-beetles were tested
within 4 days; the odour laden filter papers were replaced by new
ones for each beetle tested for a period of 5 min.
dual-choice tests in separate boxes). For both questions, we compared the leaf areas fed by the beetles.
The oviposition preferences of V- and D-beetles were compared using the Mann–Whitney U-test; we compared the oviposition preference indices calculated for V- and D-beetles according to the formula (Gabel & Thiery, 1994): (number of eggs laid
on S. viminalis – number of eggs laid on S. dasyclados)/(number
of eggs laid on S. viminalis + number of eggs laid on S. dasyclados).
All statistical analyses were performed using r, version 3.0.1
(R Foundation for Statistical Computing, Austria) with the
package stats 3.0.1 and car 2.0-19 for basic statistics and GLM,
and the package nlme 3.1-115 for GLMM.
Feeding and oviposition preference assay
To investigate (i) whether P. vulgatissima discriminates between
S. viminalis and S. dasyclados when feeding and ovipositing
and (ii) whether feeding and oviposition preferences depend
on prior experience with these host plants, dual-choice bioassays were conducted with V- and D-beetles. One twig of S.
viminalis and one of S. dasyclados were offered simultaneously to either female V-beetles or D- beetles in a transparent
plastic box (20 × 20 × 10 cm3 ; Gerda; Famos Westmark GmbH,
Germany). Each twig was 15 cm long; the mean ± SE leaf
area was 215.8 ± 7.9 cm2 (n = 11) for S. viminalis twigs and
278.9 ± 17.1 cm2 (n = 11) for S. dasyclados twigs. We placed 11
females in a box, which was closed by a lid with a gauze window
(diameter 10 cm). Females were allowed to feed and lay eggs
for 3 days. Then, we measured the leaf area consumed and the
number of eggs laid. In total, 11 replicates (boxes each with 11
females and a twig of S. dasyclados and S. viminalis) were conducted with V- and D-beetles each. The beetles in a box fed, on
average, 5–6% of the offered leaf area. They used more than
half of all leaves per box for egg deposition, although at least
40% of all leaves per twig were left egg free. Hence, beetles were
supplied with sufficient leaf material for feeding and oviposition
during the bioassays.
Results
Olfactory preference assay: beetle responses to plant
odours
Female beetles that were associated as pupae and adults with S.
dasyclados (D-beetles) significantly preferred the olfactometer
field supplied with odour of S. dasyclados leaves; they spent
significantly more time in this field than expected by the null
hypothesis (d.f. = 24, V = 242.0, P = 0.032); in contrast, they
spent less time than expected matching the null hypothesis of
equal distribution in the olfactometer field supplied with odour
of S. viminalis leaves (d.f. = 24, V = 63.0, P = 0.006) (Fig. 1a).
Female beetles maintained on S. viminalis during their entire
development (V-beetles) did not show any olfactory preference
for the host plant odours tested; they did not spend more time
in the olfactometer fields with S. viminalis or S. dasyclados
(a)
(b)
Statistical analysis
The olfactometer assay data were analyzed by the Wilcoxon
one-sample test. We tested whether the time spent by the beetles
in the olfactometer fields differed significantly from the null
hypothesis (75 s in one field of the four-chamber olfactometer,
assuming equally long residence times in all four olfactometer
fields during an observation period of 300 s).
For the statistical evaluation of the feeding preference bioassay, we addressed two questions: (i) do V-beetles (D-beetles)
feed more on S. viminalis or on S. dasyclados? (i.e. do they
show a feeding preference for either willow species?) and (ii)
do V-beetles feed more on S. viminalis (S. dasyclados) than
D-beetles? (i.e. does food uptake on a particular willow species
differ between V- and D-beetles?). We used generalized linear mixed models (GLMMs) with repeated measurements (random factor = paired samples) and gamma distribution for the
first question (dual-choice tests, dependent data) and generalized
linear models (GLMs) with gamma distribution for the second
question (independent data, D- and V-beetles were subjected to
Figure 1 Olfactory responses of female Phratora vulgatissima to (a)
odour of host plant leaves and (b) green leaf volatiles (GLV) at the ratios
1 : 1 and 1 : 3 (Z)-3-hexenol : (Z)-3-hexenyl acetate (odour mimic of Salix
viminalis: 1 : 1; Salix dasyclados: 1 : 3). V-beetles [(a) n = 22, (b) n = 25]:
experienced S. viminalis during their entire development; D-beetles [(a)
n = 25, (b) n = 28]: experienced S. dasyclados during their pupal and
adult stage. Odours were offered simultaneously (dual-choice test). Residence time (median, 25–75% percentiles, minimum/maximum) of beetles in the two opposite test fields of a static four-chamber olfactometer
during a 5-min observation period (300 s) is shown. Statistical differences
(n.s., P > 0.05; * P ≤ 0.05; **P ≤ 0.01; Wilcoxon one-sample test) to an
expected residence time (ER) (one quarter of the whole observation time
of 300 s) are given.
© 2014 The Royal Entomological Society, Agricultural and Forest Entomology, 16, 417–425
Phenotypic plasticity in host plant preference
leaf odours than in the odour-free control fields (d.f. = 21,
test chamber with S. viminalis odour: V = 140.0, P = 0.680;
test chamber with S. dasyclados odour: V = 118.0, P = 0.799)
(Fig. 1a).
(a)
Olfactory preference assay: beetle responses to GLVs
(b)
The olfactory responses by female beetles to the synthetic GLV
blends mimicking either S. viminalis or S. dasyclados leaf odour
matched their responses to the leaf odours of the tested plant
species.
Female D-beetles preferred the olfactometer field with the
GLV blend mimicking the GLV emission of S. dasyclados
leaves; they spent significantly more time in the olfactometer
field supplied with the GLV ratio (1 : 3) of S. dasyclados
leaves (d.f. = 27, V = 315.5, P = 0.011) and less time (d.f. = 27,
V = 96.0, P = 0.014) in the olfactometer chamber with the GLV
ratio (1 : 1) of S. viminalis leaves (Fig. 1b).
Female V-beetles spent approximately the same amount
of time in the odour fields supplied with GLV blends and in
the empty control fields and showed no preference for any
odour (d.f. = 25, test chamber with GLV 1 : 1 ratio: V = 185.0,
P = 0.560; test chamber with GLV 1 : 3 ratio: V = 130.0,
P = 0.396) (Fig. 1b).
Feeding and oviposition preference assay
The dual-choice feeding bioassays revealed that both Vand D-beetles preferred to feed upon S. viminalis (GLMMs,
V-beetles: d.f. = 10, t = 6.54, P < 0.001; D-beetles: d.f. = 10,
t = 2.68, P = 0.023).
Food uptake (leaf area consumed) of V- and D- beetles on
S. viminalis did not significantly differ (mean ± SE: 14.4 ± 1.5
and 13.1 ± 1.8 cm2 , respectively), neither did the leaf area of
S. dasyclados consumed by V- and D-beetles (mean ± SE:
3.3 ± 0.4 and 4.2 ± 1.1 cm2 , respectively) show any significant
differences (GLMs, S. viminalis: d.f. = 20, t = −0.52, P = 0.612;
S. dasyclados: d.f. = 20, t = 0.82, P = 0.422) (Fig. 2a).
The dual-choice oviposition bioassays showed that the oviposition preference indices of V- and D-beetles [oviposition preference index median (25/75% percentiles): 37.9 (19.5/64.4)
and 19.0 (−7.9/82.8), respectively] were not different (d.f. = 19,
U = 47, P = 0.597). Both V- and D-beetles preferred to oviposit
on leaves of S. viminalis over those of S. dasyclados (times of
positive oviposition preference indices out of all samples for
V-beetles: 10 out of 11; D-beetles:seven out of 10) (Fig. 2b).
Discussion
The present study, investigating the impact of previous experience of adult P. vulgatissima with different willow species on the
beetle’s olfactory, feeding and oviposition preferences, revealed
that olfactory preferences are mediated by experiences, whereas
feeding and oviposition preferences are independent of the experience. Regardless of the previous experience of adults with plant
species, P. vulgatissima adults preferred to feed and oviposit
on leaves of S. viminalis. Furthermore, only experience with a
421
Figure 2 (a) Feeding and (b) oviposition preference of female Phratora
vulgatissima exposed to Salix viminalis and Salix dasyclados (dual-choice
tests). V-beetles: experienced S. viminalis during their entire development; D-beetles: experienced S. dasyclados during their pupal and adult
stage. In total, 10 or 11 tests were performed each with 11 females
that could feed or oviposit on either willow species for 3 days. (a) Feeding preference: mean ± SE consumed leaf areas and the comparison
of fed leaf area of V- and D-beetles for each plant species by generalized linear models are shown; n.s., P > 0.05. (b) Oviposition preference:
median, 25–75% percentiles, minimum/maximum of oviposition preference indices and comparison of these for V- and D-beetles by the
Mann–Whitney U-test are shown; n.s., P > 0.05.
particular host species (S. dasyclados) resulted in olfactory preference for this host and the particular GLV blend mimicking the
GLV blend released by this willow species. By contrast, experience with S. viminalis did not result in any olfactory preference.
The finding that an olfactory preference was inducible for
S. dasyclados volatiles but not for S. viminalis volatiles might
be a result of the different quantities of leaf volatiles released
by these species. Undamaged S. viminalis leaves release very
few plant volatiles, whereas undamaged S. dasyclados leaves
release the GLVs (Z)-3-hexenol and (Z)-3-hexenyl acetate in
high amounts (Peacock et al., 2001). Mechanically damaged S.
dasyclados leaves emit approximately three-fold higher amounts
of volatiles in total than mechanically damaged S. viminalis
leaves (Peacock et al., 2001). The huge amount of volatiles
released from damaged S. dasyclados leaves might facilitate
experience-mediated induction of host plant preference for this
willow species.
The preference of adult beetles for a synthetic GLV blend
mimicking the ratio of the two major GLVs (Z)-3-hexenol and
(Z)-3-hexenyl acetate (1 : 3) released by S. dasyclados indicates
that a particular quantitative blend of ubiquitously occurring
volatiles may induce the olfactory preference for a host plant
species when these volatiles are released in high amounts. The
quantity of (Z)-3-hexenyl acetate was only 1.5-fold higher in
the used 1 : 3 mixture compared with the used 1 : 1 mixture.
Thus, it is unlikely that the experience of larger quantities of
a highly volatile GLV [(Z)-3-hexenyl acetate] might induce
olfactory preference for a host plant species that releases this
GLV in respective quantities. To determine the impact of GLV
quantities and ratios on olfactory preferences of P. vulgatissima,
future studies should test how the experience of adults with high
quantities of just (Z)-3-hexenyl acetate or with other ratios of
(Z)-3-hexenol and (Z)-3-hexenyl acetate affects the olfactory
preferences of this beetle. This knowledge could be used to
© 2014 The Royal Entomological Society, Agricultural and Forest Entomology, 16, 417–425
422
N. Austel et al.
employ GLVs for trapping P. vulgatissima before they reach the
willow plantation.
Electrophysiological studies (Fernandez et al., 2007) have
shown that the antenna of P. vulgatissima responds strongly to the
terpenoids R-(+)-limonene, (E/Z)-𝛽-ocimene, 𝛽-caryophyllene,
although they respond even more strongly to (Z)-3-hexenol
and (Z)-3-hexenyl acetate. Distinct ratios of GLVs also play a
major role in host plant recognition in other plant–herbivore
interactions (Bruce et al., 2005). The olfactory host plant orientation of the Colorado potato beetle Leptinotarsa decemlineata (Coleoptera: Chrysomelidae) is closely linked to the
natural GLV ratio of potato plants. The addition of synthetic
GLVs to host plant odours in unnatural ratios can disturb the
olfactory attraction of herbivorous insects to natural host plant
odours (Visser & Ave, 1978). GLVs are the key compounds
mediating host plant recognition by the leaf beetle Diorhabda
elongata (Coleoptera: Chrysomelidae) to Tamarix ramosissima
(Caryophyllales: Tamaricaceae) (Cossé et al., 2006). In the
plant–herbivore system peach Prunus persica (Rosales: Amygdaleae) and oriental fruit moth Cydia molesta (Lepidoptera: Tortricidae), only the combination of the two GLVs (Z)-3-hexenyl
acetate and (Z)-3-hexenol with benzaldehyde in a distinct ratio
of 4 : 1 : 1 mimics the attractive host plant odour, even though the
host plant bouquet is a very complex combination of 22 volatiles
(Natale et al., 2003). The importance of GLVs for the orientation
of herbivorous insects is not only limited to the location of food
resources, but also may extend even to mate finding (Reinecke
et al., 2002; Reddy & Guerrero, 2004).
The phenotypic plasticity in olfactory preferences of P. vulgatissima might be advantageous for dispersion and exploring new habitats. It allows willow leaf beetles not only to be
flexible when finding and accepting new willow species, but
also to deal with intraspecific host plant variability. Willows
show a high degree of intra- and interspecific variation in their
secondary compound content and nutritional value (Nyman &
Julkunen-Tiitto, 2005; Agren & Weih, 2012). Furthermore, willows show high inter- and intraspecific quantitative and qualitative variability in the release of volatiles (Peacock et al., 2001;
Fernandez et al., 2007; Yoneya et al., 2010). Phenotypic plasticity in plants can affect the abundance and distribution of herbivores (Agrawal, 2001). A specialized herbivore is expected to
be able to cope with these variations. P. vulgatissima feeds on a
wide range of willow species but prefers willows with a low level
of phenolglycosides, although it can cope with high amounts of
these secondary plant compounds (Peacock et al., 2004).
Because the performance of P. vulgatissima is worse on S.
dasyclados than on S. viminalis (Torp et al., 2013), the induction of an olfactory preference for S. dasyclados appears to
be maladaptive. However, the performance observed in laboratory bioassays might differ from the performance in the field.
Although beetles maintained in the laboratory are usually provided with fresh leaf material at short intervals, beetles in the field
usually feed continuously on a tree that starts to defend against
severe herbivore damage by systemic feeding-induced defence
responses (Ruuhola et al., 2001; Dalin & Björkman, 2003). Furthermore, the benefit gained by the preference of a particular
host plant species over another might depend not only on the
nutritional value of the compared plant species, but also on the
extent of interspecific competition and enemy pressure that will
be experienced on these plant species (Hunter & Price, 1992). It
has been shown that Anthocoris nemorum, an important predator
of P. vulgatissima eggs and larvae, prefers and performs better
on S. dasyclados than on S. viminalis plant material (Stenberg
et al., 2010, 2011a) and that the predator is more prone to feed
on eggs and larvae on S. viminalis than on S. dasyclados (Stenberg et al., 2011b). The interaction of the factors plant defence,
nutritional value, interspecific competition and enemy pressure,
which vary in strength at different sites and with abiotic conditions, can affect the performance of P. vulgatissima on S. viminalis and S. dasyclados in the field.
By contrast to the olfactory preferences for a host plant, feeding and oviposition preferences of P. vulgatissima were not
affected by prior experience with a host plant. Regardless of
the plant species that had been experienced as adults, females
showed strong feeding and oviposition preferences for S. viminalis over S. dasyclados. Feeding and oviposition preferences
might be genetically fixed in the tested beetles or might have
developed during larval experience with S. viminalis (both V- and
D-beetles experienced S. viminalis during larval development).
According to the ‘mother knows best’ principle or the preference/performance theory (Jaenike, 1978; Thompson, 1988;
Gripenberg et al., 2010; Wennström et al., 2010), oviposition is
considered as a very crucial step of the host plant selection process (Schoonhoven et al., 2005a). The phenomenon of innate
oviposition preference behaviour that shows low phenotypic
plasticity has also been observed in several other Coleopteran
species. When the mustard leaf beetle Phaedon cochleariae
(Coleoptera: Chrysomelidae) was reared on a novel host plant
species for 10 generations and more, the beetle changed its
feeding behaviour but not its oviposition behaviour (Kühnle &
Müller, 2011). Similarly, when P. cochleariae larvae were fed on
either old or young leaves of Brassica rapa, the resulting females
always preferred to oviposit on young leaves that contained lower
concentrations of glucosinolates and thus were of higher quality
than older leaves, regardless of their feeding experience during
the larval stage (Tremmel & Müller, 2013). However, several
other studies on different herbivorous species showed that oviposition preferences for specific host plants are also inducible by
prior (larval and adult) experience with the plant (Coyle et al.,
2011; Anderson et al., 2013). Future studies need to determine
which environmental conditions, plant traits and intrinsic factors
of insects favour (experience-mediated) phenotypic plasticity of
oviposition and feeding preferences in herbivorous insects.
The results of the present study indicate a decrease in
behavioural plasticity from (olfactory) long range orientation
towards host trees to short range orientation and the final host
acceptance for oviposition. Olfactory preferences might be especially important when the beetles start to colonize trees in spring.
Because phenotypic plasticity in olfactory host location can
reduce the success of management efforts that employ plant
volatiles for manipulation of pest insect behaviour, knowledge
on the chemical composition of the odours of willow species, on
the olfactory responses of the leaf beetle population in focus and
on the conditions that shape the plant odours and beetle responses
may help to improve biocontrol efficiency. Exposure of beetles to odour of stands with various willow species might affect
experience-induced olfactory preference for a single species and
© 2014 The Royal Entomological Society, Agricultural and Forest Entomology, 16, 417–425
Phenotypic plasticity in host plant preference
thus impair host location success. Future studies should investigate how experience-mediated induction of olfactory preferences for S. dasyclados or other willow species can contribute to
the reduction of P. vulgatissima population densities in willow
stands.
Acknowledgements
This work was supported by the Scholarship Programme of
the German Federal Environmental Foundation, the Dahlem
Research School of the Freie Universität Berlin (N.A.) and
partly by the Salix Molecular Breeding Activities (SAMBA)
project (C.B.), which was funded by the Swedish Energy Agency,
Swedish University of Agricultural Sciences (SLU) and Lantmännen SW Seed.
References
Agrawal, A.A. (2001) Ecology – phenotypic plasticity in the interactions
and evolution of species. Science, 294, 321–326.
Agren, G.I. & Weih, M. (2012) Plant stoichiometry at different scales:
element concentration patterns reflect environment more than genotype. New Phytologist, 194, 944–952.
Åhman, I., Glinwood, R. & Ninkovic, V. (2010) The potential for modifying plant volatile composition to enhance resistance to arthropod
pests. CAB Reviews, 5, 1–10.
Anderson, P., Sadek, M.M., Larsson, M., Hansson, B.S. & Thöming, G.
(2013) Larval host plant experience modulates both mate finding and
oviposition choice in a moth. Animal Behaviour, 85, 1169–1175.
Anton, S., Dufour, M.C. & Gadenne, C. (2007) Plasticity of
olfactory-guided behaviour and its neurobiological basis: lessons
from moths and locusts. Entomologia Experimentalis et Applicata,
123, 1–11.
Bach, C.E. (1994) Effects of herbivory and genotype on growth and
survivorship of sand-dune willow (Salix cordata). Ecological Entomology, 19, 303–309.
Barron, A.B. (2001) The life and death of Hopkins’ host-selection
principle. Journal of Insect Behavior, 14, 725–737.
Bernays, E.A. & Chapman, R.F. (1994) Host-plant Selection by Phytophagous Insects. Chapman and Hall, New York, New York.
Bernays, E.A. & Weiss, M.R. (1996) Induced food preferences in caterpillars: the need to identify mechanisms. Entomologia Experimentalis
et Applicata, 78, 1–8.
Beyaert, I. & Hilker, M. (2014) Plant odour plumes as mediators of
plant–insect interactions. Biological Reviews, 89, 68–81.
Björkman, C. & Eklund, K. (2006) Factors affecting willow leaf beetles
(Phratora vulgatissima) when selecting overwintering sites. Agricultural and Forest Entomology, 8, 97–101.
Björkman, C., Höglund, S., Eklund, K. & Larsson, S. (2000) Effects
of leaf beetle damage on stem wood production in coppicing willow.
Agricultural and Forest Entomology, 2, 131–139.
Bruce, T.J.A. & Pickett, J.A. (2011) Perception of plant volatile blends
by herbivorous insects – finding the right mix. Phytochemistry, 72,
1605–1611.
Bruce, T.J.A., Wadhams, L.J. & Woodcock, C.M. (2005) Insect host
location: a volatile situation. Trends in Plant Science, 10, 269–274.
Corbet, S.A. (1985) Insect chemosensory responses: a chemical legacy
hypothesis. Ecological Entomology, 10, 143–153.
Cossé, A.A., Bartelt, R.J., Zilkowski, B.W., Bean, D.W. & Andress, E.R.
(2006) Behaviorally active green leaf volatiles for monitoring the leaf
beetle, Diorhabda elongata, a biocontrol agent of saltcedar, Tamarix
spp. Journal of Chemical Ecology, 32, 2695–2708.
423
Courtney, S.P. & Kibota, T.T. (1990) Mother doesn’t know best: selection
of hosts by ovipositing insects. Insect–Plant Interactions, Vol. 2 (ed.
by E.A. Bernays), pp. 161–188. CRC Press, Boca Raton, Florida.
Courtney, S.P., Chen, G.K. & Gardner, A. (1989) A general model for
individual host selection. Oikos, 55, 55–65.
Coyle, D.R., Clark, K.E., Raffa, K.F. & Johnson, S.N. (2011) Prior host
feeding experience influences ovipositional but not feeding preference
in a polyphagous insect herbivore. Entomologia Experimentalis et
Applicata, 138, 137–145.
Cunningham, J.P., Jallow, M.F.A., Wright, D.J. & Zalucki, M.P. (1998)
Learning in host selection in Helicoverpa armigera (Hubner) (Lepidoptera: Noctuidae). Animal Behaviour, 55, 227–234.
Dalin, P. & Björkman, C. (2003) Adult beetle grazing induces willow
trichome defence against subsequent larval feeding. Oecologia, 134,
112–118.
Davidson, M.M., Butler, R.C. & Teulon, D.A.J. (2006) Starvation period
and age affect the response of female Frankliniella occidentalis
(Pergande) (Thysanoptera: Thripidae) to odor and visual cues. Journal
of Insect Physiology, 52, 729–736.
Davis, J.M. (2008) Patterns of variation in the influence of natal
experience on habitat choice. Quarterly Review of Biology, 83,
363–380.
Davis, J.M. & Stamps, J.A. (2004) The effect of natal experience on
habitat preferences. Trends in Ecology & Evolution, 19, 411–416.
Dethier, V.G. (1982) Mechanism of host-plant recognition. Entomologia
Experimentalis et Applicata, 31, 49–56.
Devaud, J.M., Acebes, A., Ramaswami, M. & Ferrus, A. (2003) Structural and functional changes in the olfactory pathway of adult
Drosophila take place at a critical age. Journal of Neurobiology, 56,
13–23.
Diehl, S.R. & Bush, G.L. (1984) An evolutionary and applied perspective
of insect biotypes. Annual Review of Entomology, 29, 471–504.
Ehrlich, P.R. & Raven, P.H. (1964) Butterflies and plants: a study in
coevolution. Evolution, 18, 586–608.
Fernandez, P. & Hilker, M. (2007) Host plant location by Chrysomelidae.
Basic and Applied Ecology, 8, 97–116.
Fernandez, P.C., Meiners, T., Björkman, C. & Hilker, M. (2007) Electrophysiological responses of the blue willow leaf beetle, Phratora
vulgatissima, to volatiles of different Salix viminalis genotypes. Entomologia Experimentalis et Applicata, 125, 157–164.
Futuyma, D.J. & McCafferty, S.S. (1990) Phylogeny and the evolution of
host plant associations in the leaf beetle genus Ophraella (Coleoptera,
Chrysomelidae). Evolution, 44, 1885–1913.
Gabel, B. & Thiery, D. (1994) Semiochemicals from Lobesia botrana
(Lepidoptera, Tortricidae) eggs deter oviposition by the codling moth
Cydia pomonella (Lepidoptera, Tortricidae). European Journal of
Entomology, 91, 353–359.
Gripenberg, S., Mayhew, P.J., Parnell, M. & Roslin, T. (2010) A
meta-analysis of preference–performance relationships in phytophagous insects. Ecology Letters, 13, 383–393.
Harari, A.R. & Landolt, P.J. (1999) Feeding experience enhances attraction of female Diaprepes abbreviatus (L.) (Coleoptera: Curculionidae)
to food plant odors. Journal of Insect Behavior, 12, 415–422.
Hopkins, A.D. (1917) A discussion of C. G. Hewitt’s paper on ‘Insect
Behaviour’. Journal of Economic Entomology, 10, 92–93.
Hunter, M.D. & Price, P.W. (1992) Playing chutes and ladders: heterogeneity and the relative roles of bottom-up and top-down forces in
natural communities. Ecology, 73, 724–732.
Jaenike, J. (1978) On optimal oviposition behavior in phytophagous
insects. Theoretical Population Biology, 14, 350–356.
Jaenike, J. (1983) Induction of host preference in Drosophila
melanogaster. Oecologia, 58, 320–325.
Jaenike, J. (1990) Host specialisation in phytopagous insects. Annual
Review of Ecology and Systematics, 21, 243–273.
© 2014 The Royal Entomological Society, Agricultural and Forest Entomology, 16, 417–425
424
N. Austel et al.
Jallow, M.F.A., Cunningham, J.P. & Zalucki, M.P. (2004) Intra-specific
variation for host plant use in Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae): implications for management. Crop Protection,
23, 955–964.
Julkunen-Titto, R. (1989) Phenolic constituents of Salix – a chemotaxonomic survey of further finnish species. Phytochemistry, 28,
2115–2125.
Karp, A. & Peacock, L. (2004) The ecology and population genetics
of the blue and brassy willow beetles (Phyllodecta (=Phratora) vulgatissmina L.) and P. vitellinae L. on United Kingdom willow (Salix)
plantations. New Developments in the Biology of Chrysomelidae (ed.
by P. Jolivet, J. A. Santiago-Blay and M. Schmitt), pp. 97-104. SPB
Academic Publishing BV, The Netherlands.
Kelly, M.T. & Curry, J.P. (1991) The infuence of phenolic compounds on
the suitability of 3 Salix species as host for the willow beetle Phratora
vulgatissima. Entomologia Experimentalis et Applicata, 61, 25–32.
Kendall, D.A. & Wiltshire, C.W. (1998) Life-cycles and ecology of
willow beetles on Salix viminalis in England. European Journal of
Forest Pathology, 28, 281–288.
Kendall, D.A., Hunter, T., Arnold, G.M., Liggitt, J., Morris, T. &
Wiltshire, C.W. (1996) Susceptibility of willow clones (Salix spp) to
herbivory by Phyllodecta vulgatissima (L) and Galerucella lineola
(Fab) (Coleoptera, Chrysomelidae). Annals of Applied Biology, 129,
379–390.
Koschier, E.H., De Kogel, W.J. & Visser, J.H. (2000) Assessing
the attractiveness of volatile plant compounds to western flower
thrips Frankliniella occidentalis. Journal of Chemical Ecology, 26,
2643–2655.
Kühnle, A. & Müller, C. (2011) Responses of an oligophagous beetle
species to rearing for several generations on alternative host-plant
species. Ecological Entomology, 36, 125–134.
Larsson, S. (1983) Effects of artificial defoliation on stem growth in Salix
smithiana grown under intensive culture. Acta Oecologica, Oecologia
Applicata, 4, 343–349.
Lehrman, A., Torp, M., Stenberg, J.A., Julkunen-Tiitto, R. & Bjorkman,
C. (2012) Estimating direct resistance in willows against a major
insect pest, Phratora vulgatissima, by comparing life history traits.
Entomologia Experimentalis et Applicata, 144, 93–100.
Liu, S.S., Li, Y.H., Liu, Y.Q. & Zalucki, M.P. (2005) Experience-induced
preference for oviposition repellents derived from a non-host plant by
a specialist herbivore. Ecology Letters, 8, 722–729.
Mallon, E.B., Brockmann, A. & Schmid-Hempel, P. (2003) Immune
response inhibits associative learning in insects. Proceedings of
the Royal Society of London Series B, Biological Sciences, 270,
2471–2473.
Menzel, R. & Müller, U. (1996) Learning and memory in honeybees:
from behavior to neural substrates. Annual Review of Neuroscience,
19, 379–404.
Natale, D., Mattiacci, L., Hern, A., Pasqualini, E. & Dorn, S. (2003)
Response of female Cydia molesta (Lepidoptera: Tortricidae) to plant
derived volatiles. Bulletin of Entomological Research, 93, 335–342.
Nyman, T. & Julkunen-Tiitto, R. (2005) Chemical variation within and
among six northern willow species. Phytochemistry, 66, 2836–2843.
Peacock, L., Herrick, S. & Brain, P. (1999) Spatio-temporal dynamics
of willow beetle (Phratora vulgatissima) in short-rotation coppice
willows grown as monocultures or a genetically diverse mixture.
Agricultural and Forest Entomology, 1, 287–296.
Peacock, L., Lewis, M. & Powers, S. (2001) Volatile compounds from
Salix spp. varieties differing in susceptibility to three willow beetle
species. Journal of Chemical Ecology, 27, 1943–1951.
Peacock, L., Carter, P., Powers, S. & Karp, A. (2003) Geographic
variation in phenotypic traits in Phratora spp. and the effects of
conditioning on feeding preference. Entomologia Experimentalis et
Applicata, 109, 31–37.
Peacock, L., Harris, J. & Powers, S. (2004) Effects of host variety on blue
willow beetle Phratora vulgatissima performance. Annals of Applied
Biology, 144, 45–52.
Peng, Y. & Wang, Y.F. (2009) Infection of Wolbachia may improve
the olfactory response of Drosophila. Chinese Science Bulletin, 54,
1369–1375.
Prokopy, R. & Lewis, W.J. (1993) Application of learning to pest
management. Insect Learning (ed. by D. Papaj and A. Lewis), pp.
308-342. Springer, The Netherlands.
Prokopy, R.J., Averill, A.L., Cooley, S.S. & Roitberg, C.A. (1982)
Associative learning in egglaying site selection by apple maggot flies.
Science, 218, 76–77.
Radžiutė, S. & Būda, V. (2012) Host feeding experience affects host plant
odour preference of the polyphagous leafminer Liriomyza bryoniae.
Entomologia Experimentalis et Applicata, 146, 286–292.
Reddy, G.V.P. & Guerrero, A. (2004) Interactions of insect pheromones
and plant semiochemicals. Trends in Plant Science, 9, 253–261.
Reinecke, A., Ruther, J., Tolasch, T., Francke, W. & Hilker, M. (2002)
Alcoholism in cockchafers: orientation of male Melolontha melolontha towards green leaf alcohols. Naturwissenschaften, 89, 265–269.
Ruuhola, T.M., Sipura, M., Nousiainen, O. & Tahvanainen, J. (2001)
Systemic induction of salicylates in Salix myrsinifolia (Salisb.). Annals
of Botany, 88, 483–497.
Sage, R.B. & Tucker, K. (1997) Invertebrates in the canopy of willow
and poplar short rotation coppices. Aspects of Applied Biology, 49,
105–111.
Sage, R.B. & Tucker, K. (1998) The distribution of Phratora vulgatissima (Coleoptera: Chrysomelidae) on cultivated willows in
Britain and Ireland. European Journal of Forest Pathology, 28,
289–296.
Santana, A.F.K. & Zucoloto, F.S. (2011) Influence of previous experience
on the preference, food utilization and performance of Ascia monuste
orseis wild larvae (Godart) (Lepidoptera: Pieridae) for three different
hosts. Neotropical Entomology, 40, 631–638.
Saxena, K.N. & Schoonhoven, L.M. (1982) Induction of orientational and feeding prefernces in Manduca sexta larvae for different food sources. Entomologia Experimentalis et Applicata, 32,
173–180.
Schoonhoven, L.M., Van Loon, J.J.A. & Dicke, M. (2005a) Host-plant
selection: how to find a host plant. Insect–Plant Biology (ed. by L. M.
Schoonhoven, J. J. A. Van Loon and M. Dicke), pp. 135-168. Oxford
University Press, U.K.
Schoonhoven, L.M., Van Loon, J.J.A. and Dicke, M. (2005b) Host-plant
selection: variation is the rule. Insect–Plant Biology (ed. by L. M.
Schoonhoven, J. J. A. Van Loon and M. Dicke), pp. 209-232. Oxford
University Press, U.K.
Schoonhoven, L.M., Van Loon, J.J.A. & Dicke, M. (2005c) Insects and
plants: how to apply our knowledge. Insect–Plant Biology (ed. by
L. M. Schoonhoven, J. J. A. Van Loon and M. Dicke), pp. 336-363.
Oxford University Press, U.K.
Smith, M.A. & Cornell, H.V. (1979) Hopkins host-selection in Nasonia
vitripennis and its implications for sympathic speciation. Animal
Behaviour, 27, 365–370.
Steidle, J.L.M. & Schöller, M. (1997) Olfactory host location and
learning in the granary weevil parasitoid Lariophagus distinguendus (Hymenoptera: Pteromalidae). Journal of Insect Behavior, 10,
331–342.
Stenberg, J.A., Lehrman, A. & Björkman, C. (2010) Uncoupling direct
and indirect plant defences: novel opportunities for improving crop
security in willow plantations. Agriculture, Ecosystems & Environment, 139, 528–533.
Stenberg, J.A., Lehrman, A. & Björkman, C. (2011a) Host-plant genotype mediates supply and demand of animal food in an omnivorous
insect. Ecological Entomology, 36, 442–449.
© 2014 The Royal Entomological Society, Agricultural and Forest Entomology, 16, 417–425
Phenotypic plasticity in host plant preference
Stenberg, J.A., Lehrman, A. & Björkman, C. (2011b) Plant defence:
feeding your bodyguards can be counter-productive. Basic and
Applied Ecology, 12, 629–633.
Szendrei, Z. & Rodriguez-Saona, C. (2010) A meta-analysis of insect
pest behavioral manipulation with plant volatiles. Entomologia Experimentalis et Applicata, 134, 201–210.
Thiery, D. & Visser, J.H. (1995) Satiation effects on olfactory orientation
patterns of Colorado potato beetle females. Comptes Rendus de l
Academie des Sciences Serie III – Sciences de la Vie-Life Sciences,
318, 105–111.
Thompson, J.N. (1988) Evolutionary ecology of the relationship
between oviposition preference and performance of offspring in
phytophagous insects. Entomologia Experimentalis et Applicata, 47,
3–14.
Torp, M., Lehrman, A., Stenberg, J.A., Julkunen-Tiitto, R. & Bjorkman,
C. (2013) Performance of an herbivorous leaf beetle (Phratora
vulgatissima) on Salix F2 hybrids: the importance of phenolics.
Journal of Chemical Ecology, 39, 516–524.
425
Tremmel, M. & Müller, C. (2013) The consequences of alternating
diet on performance and food preferences of a specialist leaf beetle.
Journal of Insect Physiology, 59, 840–847.
Visser, J.H. & Ave, D.A. (1978) General green leaf volatiles in the olfactory orientation of the Colorado beetle, Leptinotarsa decemlineata.
Entomologia Experimentalis et Applicata, 24, 738–749.
Walter, G.H. (2003) Insect Pest Management and Ecological Research.
Cambridge University Press, New York, New York.
Wennström, A., Hjulstrom, L.N., Hjalten, J. & Julkunen-Tiitto, R. (2010)
Mother really knows best: host choice of adult phytophagous insect
females reflects a within-host variation in suitability as larval food.
Chemoecology, 20, 35–42.
Yoneya, K., Ozawa, R. & Takabayashi, J. (2010) Specialist leaf beetle
larvae use volatiles from willow leaves infested by conspecifics for
reaggregation in a tree. Journal of Chemical Ecology, 36, 671–679.
Accepted 18 April 2014
First published online 27 May 2014
© 2014 The Royal Entomological Society, Agricultural and Forest Entomology, 16, 417–425