Journal of Plant Interactions
ISSN: 1742-9145 (Print) 1742-9153 (Online) Journal homepage: http://www.tandfonline.com/loi/tjpi20
Interaction–information networks mediated by
plant volatiles: a case study on willow trees
Kinuyo Yoneya & Junji Takabayashi
To cite this article: Kinuyo Yoneya & Junji Takabayashi (2013) Interaction–information networks
mediated by plant volatiles: a case study on willow trees, Journal of Plant Interactions, 8:3,
197-202, DOI: 10.1080/17429145.2013.782514
To link to this article: http://dx.doi.org/10.1080/17429145.2013.782514
Copyright Taylor and Francis Group, LLC
Accepted author version posted online: 04
Mar 2013.
Published online: 14 Apr 2013.
Submit your article to this journal
Article views: 316
View related articles
Citing articles: 6 View citing articles
Full Terms & Conditions of access and use can be found at
http://www.tandfonline.com/action/journalInformation?journalCode=tjpi20
Download by: [5.10.31.130]
Date: 16 June 2017, At: 02:44
Journal of Plant Interactions, 2013
Vol. 8, No. 3, 197202, http://dx.doi.org/10.1080/17429145.2013.782514
REVIEW ARTICLE
Interaction information networks mediated by plant volatiles: a case study on willow trees
Kinuyo Yoneya and Junji Takabayashi*
Center for Ecological Research, Kyoto University, Otsu 520-2113, Japan
(Received 31 January 2013; accepted 2 March 2013)
Volatiles from uninfested plants as well as those from plants infested by herbivores have been reported to
potentially contain information that can be used by herbivorous arthropods, their carnivorous natural enemies,
and plants. In this context, tritrophic interactioninformation networks are expected. Here, as a case study of
such a volatile-mediated network, we reviewed our recent studies on a naturally occurring tritrophic system of a
willow tree (Salix eriocarpa), a leaf beetle (Plagiodera versicolora), and a predatory ladybird (Aiolocaria
hexaspilota) mediated by volatiles from uninfested and infested willow trees. Ecological functions of uninfested
and infested willow-shoot volatiles depended on receivers (i.e. leaf beetle adults, leaf beetle larvae, ladybirds, and
conspecific tree). By studying such multifunctional aspects of plant volatiles in different natural willow fields, we
would acquire a more comprehensive understanding of interactioninformation networks.
Keywords: willow tree; willow leaf beetle; ladybird; Plagiodera versicolora; Aiolocaria hexaspilota; Salix
eriocarpa
Introduction
Uninfested plants of different species emit different
blends of volatile organic compounds that are used not
only by herbivores but also by foraging carnivores (e.g.
Takabayashi et al. 1991; Baur et al. 1993; Shiojiri et al.
2002). Furthermore, in response to biotic stresses such
as herbivory and pathogen infection, plants are known
to emit specific blends of volatiles. When infested by
herbivorous arthropods, plants emit the so-called
‘herbivore-induced plant volatiles (HIPVs)’ whose
blends are specific not only to the herbivore species,
developmental stage, and number on the plant, but
also to the plant species, plant developmental stage,
etc. (e.g. Takabayashi & Dicke, 1996; Arimura et al.
2009). Thus, such blends can convey specific information about plant condition.
Several carnivorous natural enemies of herbivores
are known to use such specific information in HIPVs
(e.g. Takabayashi et al. 1995; De Moraes et al. 1998;
Du et al. 1998; Turlings et al. 1998; Guerrieri et al.
1999; Horiuchi et al. 2003; Shiojiri et al. 2010). When
natural enemies are attracted to HIPVs and consequently decrease herbivore damage levels, the emission of HIPVs is considered to be signal-based
induced indirect defense of plants against herbivores
(Yoneya et al. 2012). Furthermore, neighboring
plants eavesdrop on such volatiles as indicators of
‘clear and present danger’ and start/prime their own
direct or indirect defenses (e.g. Arimura et al. 2000,
2009; Choh et al. 2004; Engelberth et al. 2004). For
example, Choh et al. (2004) reported that uninfested
receiver plants produced more carnivore-attracting
HIPVs than did uninfested unexposed plants. Similar
*Corresponding author. Email: [email protected]
# 2013 Taylor & Francis
results were also reported in maize (Engelberth et al.
2004). Thus, imminent tritrophic interactions of
plants, herbivores, and carnivores on the eavesdroppers would not be the same as those on noneavesdropping plants. Note that this eavesdropping is not
‘interaction’ but ‘information transfer’, when the
eavesdropping plants do not affect the emitter plants.
Taken together, in this paper, we used a term
‘interactioninformation networks’ to describe ecological communities mediated by plant volatiles. Such
a volatile-mediated network is composed of three
layers that are affecting each other: trophic interactions (food webs), natural enemyplant indirect
interactions, and plantplant signaling. This idea is
schematically shown in Figure 1.
Interactioninformation networks are better evaluated in naturally occurring insectplant interactions.
However, most of the studies on the multifunctional
aspects of plant volatiles have been conducted using
crops. As a case study of plantarthropod interactions in a natural ecosystem, we focused on the
tritrophic interaction of a willow tree (Salix eriocarpa
Fr. & Sav.), a leaf beetle (Plagiodera versicolora
Laicharting), and a predatory ladybird (Aiolocaria
hexaspilota Hope) under natural conditions in Japan
(Yoneya et al. 2009a, 2009b, 2010, 2012).
Biology of willow trees, willow leaf beetles, and
ladybirds
Salix eriocarpa is a species of willow native to the wet
lowlands of Japan. S. eriocarpa is reported to reproduce
only asexually (Kimura 1989). P. versicolora, which is
198
K. Yoneya and J. Takabayashi
Figure 1. Scheme of interactioninformation networks. Gray arrows in layer 3 mean herbivore-induced plant volatile information
transfer. The first layer [layer 1: trophic interactions (food web)], the second layer (layer 2: natural enemyplant indirect
interactions), and the third layer (layer 3: plantplant signaling) are affecting each other. For example, in layer 3, the receiver
plants (eavesdroppers) become more defended against herbivores, and thus the food webs and natural enemyplant indirect
interactions that would be built on the eavesdropping plants are not the same as ones built on non-eavesdropping plants.
widely distributed across Asia, Europe, and northern
Africa (Hood 1940; Kimoto & Takizawa 1994), is a
specialist herbivore whose mobile stages all feed on
leaves of Salicaceae plants. Both larvae and adults of the
ladybird A. hexaspilota are specialist predators of eggs
and larvae of P. versicolora as well as of Chrysomela
vigintipunctata and Gastrolina depressa. A. hexaspilota
occurs in Japan, Taiwan, southern China, the Himalayas, and northern India (Kurosawa et al. 1985).
Volatiles emitted by willow plants that were uninfested
or infested by leaf beetles
We found a total of 17 volatile compounds in the
headspaces of S. eriocarpa plants that were infested
by leaf beetle larvae or adults (Table 1). The compounds (Z)-3-hexen-1-ol, (Z)-3-hexenyl acetate, benzaldehyde, and (E)-b-ocimene were common to the
volatiles emitted by uninfested and infested plants,
whereas 13 compounds were emitted only by infested
plants. The leaf areas damaged by adults and larvae
were adjusted to be the same. Plants infested by
larvae produced more volatiles, as measured by gas
chromatographymass spectrometry, than those infested by adults, and uninfested plants produced the
smallest amount. The compositions of all volatile
compounds differed significantly among the three
treatments (Yoneya et al. 2009b).
Do HIPVs inform predatory insects about the most
suitable stage of its prey?
Both the larval and adult stages of the ladybirds are
dominant natural enemies of the leaf beetle larvae. To
understand the prey-finding behavior of the ladybirds, we studied the olfactory responses of both
adults and larvae in a Y-tube olfactometer (Yoneya
et al. 2009b; Figure 2). The adults preferred undamaged willow-shoot volatiles over clean air
(Yoneya et al. 2012). While the adults showed no
preference for willow plants infested by leaf beetle
adults (non-prey) over uninfested plants, but were
more attracted to plants infested by leaf beetle
larvae (prey) than to uninfested plants. By contrast,
the ladybird larvae showed no preference for plants
infested by either leaf beetle larvae or adults over
uninfested plants.
Using gas chromatographymass spectrometry,
we found that six volatile compounds ((E)-b-ocimene,
(Z)-b-ocimene, allo-ocimene, (E,E)-a-farnesene, and
two oxime-like compounds) were released in larger
amounts in the headspaces of plants infested by leaf
beetle larvae than in those of plants infested by leaf
beetle adults (Table 1). These compounds were
candidate attractants for adult ladybugs. In addition,
the total amounts of volatiles emitted from willow
plants that were either uninfested or infested by leaf
beetle adults was less than one-tenth of that from
willow plants infested by leaf beetle larvae (Table 1).
These results indicated that volatiles from S. eriocarpa
infested by P. versicolora informed A. hexaspilota
adults about the presence and life stage of their prey,
while the ladybird larvae did not use such information
because they do not move between trees. Thus, willow
plants emit HIPVs that attract the right predators at
the right time and place for signal-based induced
indirect defense.
199
Journal of Plant Interactions
Table 1. Comparison of peak areas of volatiles detected in the headspaces of Salix eriocarpa plants that were uninfested or
infested by larvae or adults of Plagiodera versicolora.
Peak area (range)1
Compound name
Uninfested shoot
Shoot infested by adults
A. Compounds commonly found in all three treatments2
(Z)-3-Hexen-1-ol
0.0 (0.00.0) a3
2.2 (1.39.1) ab
(Z)-3-Hexenyl acetate
7.5 (1.112.3) a
7.8 (5.414.7) a
Benzaldehyde
0.0 (0.00.9) a
2.2 (0.94.0) a
(E)-b-Ocimene
0.3 (0.01.4) a
28.1 (2.044.0) b
B. Compounds found in the infested plants but not in uninfested shoots*
(E)-2-Hexenal
0.05 (0.013.0)
Salicylaldehyde
3.7 (0.08.9)
(Z)-b-Ocimene
4.8 (4.16.5)
allo-Ocimene
0.7 (0.60.9)
Linalool
0.3 (0.01.6)
(E)-DMNT4
3.0 (1.24.0)
(E)-DMOT5
2.5 (1.63.1)
(E,E)-a-Farnesene
0.2 (0.00.9)
Oxime-like compound 1
9.9 (0.012.4)
Oxime-like compound 2
5.3 (0.07.5)
Oxime-like compound 3
0.8 (0.02.3)
Unidentified compound 1
19.4 (1.529.0)
Unidentified compound 2
4.6 (0.016.9)
Shoot infested by larvae
10.7
23.3
2.5
130.2
2.0
10.6
12.2
2.1
0.5
6.1
5.1
1.3
30.6
17.3
3.2
20.8
7.8
(8.615.0) b
(12.138.0) a
(1.410.3) a
(78.0211.4) c
(1.36.3)**, ***
(4.635.8)
(6.515.0)*
(1.84.1)*
(0.01.0)
(3.17.8)
(2.45.4)**,$
(0.92.4)*
(19.951.8)*
(9.825.0)*
(2.27.5)
(11.132.8)
(0.014.2)
1
Median (interquartile range) ( 10 2).
Different letters in the same line indicate a significant difference by the SteelDwass test (P B0.05).
3
(Z)-3-Hexen-1-ol was detected from one sample of six uninfested plants (peak area: 0.029).
4
(E)-4,8-Dimethyl-1,3,7-nonatriene.
5
(E)-2.6-Dimethyl-1,3,5,7-octatetraene.
*Significantly different by the MannWhitney U-test at 0.05 P0.01.
**Marginally significantly different.
***P0.053.
$
P 0.054.
2
Figure 2. Tritrophic interactioninformation networks of willow plants (Salix eriocarpa), willow leaf beetles (Plagiodera
versicolora), and ladybirds (Aiolocaria hexaspilota). Solid lines with arrowheads indicate attraction, and dotted lines
with square heads indicate non-attraction. Triple solid lines with arrowheads denote information transfer to a neighboring
plant.
200
K. Yoneya and J. Takabayashi
Is there a trade-off between direct and signal-based
induced indirect defense against herbivores in willow
trees?
In signal-based induced indirect defense, the plants
themselves do not produce a specific reward for the
carnivores. Rather, the herbivores on the plant are
the reward. As the goal of both direct defense and
signal-based indirect defense is to minimize the
number of herbivores, important factors for carnivores participating in a signal-based induced indirect
defense response are whether the number and species
of herbivores on the plant constitute a sufficient
reward. To clarify the relative significance of direct
and signal-based induced indirect defenses in plants,
we studied tritrophic systems consisting of six sympatric willow species as well as willow leaf beetles and
ladybirds (Yoneya et al. 2012).
The relative preferences of ladybirds for preyinfested willow plant volatiles (levels of signal-based
induced indirect defense) were positively correlated
with the vulnerability of willow species to leaf beetles
(relative levels of direct defense), suggesting a resourcelimited trade-off among the species between direct
and signal-based induced indirect defense. However,
the suggested trade-off in resource limitation was
apparent because the specificity of the infested-plant
volatile blends (a factor determining the costs of
signal-based induced indirect defense) did not relate
to the levels of signal-based induced indirect defense
(for a more elaborate discussion, see Yoneya et al.
2012). This ‘apparent trade-off’ between direct and
signal-based induced indirect defense was partially
explained by differential preferences of ladybirds for
infested plant volatiles of the six willow species. The
relative preference of predators for species-specific
prey-infested plant volatiles and the community
structure of preyfood plants would be important
factors in the evolution of signal-based induced
indirect defense.
Do adult leaf beetles discriminate between volatiles
from uninfested and infested willow shoots?
We investigated how adult willow leaf beetles find
shoots with new leaves, their optimal food, by
focusing on shoot volatiles (Yoneya et al. 2009a;
Figure 2). Adults preferentially fed on young leaves
(Nakamura et al. 2003). Raupp and Sadof (1989)
found that adults did not consume all of a leaf;
rather, they ate part of it then moved to an
undamaged leaf on the same shoot. They also showed
that adults flew to another part of the same tree or to
a different tree to feed after they had used several new
leaves on a single shoot. An unresolved question is
how the beetles find shoots with uninfested new
leaves, given that these shoots are patchily distributed
in their habitat.
We used a Y-tube olfactometer to test the
olfactory preferences of adult leaf beetles. Both
females and males (either starved or satiated) preferred the volatiles of newly emerged shoots of
S. eriocarpa to clean air, indicating that they used
uninfested-shoot volatiles to find patchily distributed
food. Interestingly, in comparisons between volatiles
from uninfested shoots and those with leaves infested
by conspecific adults, starved females preferred
infested-shoot volatiles (Yoneya et al. 2009a). When
starved, females broadened their olfactory responses
to include infested-shoot volatiles to find food.
Starved males showed a similar preference, but it
did not reach a significant level. We also tested the
responses of leaf beetle adults to conspecific-larvaeinfested shoot volatiles and found that starved males
and females had no preference for either uninfestedor infested-shoot volatiles (Yoneya, unpublished).
These data showed that adult leaf beetles use both
uninfested and conspecific-adult-infested shoot volatiles to find patchily distributed shoots.
Do specialist leaf beetle larvae use volatiles from willow
leaves infested by conspecifics?
Young larvae of willow leaf beetles exhibit characteristic gregarious behavior on host trees. Larvae remain
aggregated on the natal leaf for 15 d (Crowe 1995).
Thereafter they move singly from the natal leaf to
other leaves, and reaggregate on a new leaf within a
few hours of dispersal (Wade & Breden 1986; Crowe
1995). We investigated whether plant volatiles induced by feeding P. versicolora larvae were involved
in the reaggregation behavior (Yoneya et al. 2010;
Figure 2). Under laboratory conditions, we conducted leaf disc bioassays and found that the first
and second instars discriminated between volatiles
from leaves infested by larvae versus from uninfested
leaves. The discriminative behavior depended on both
the time leaves were infested and the age of discriminating larvae. First and second instars preferred
volatiles from 1-d-infested leaves to volatiles from
uninfested leaves, whereas third instars (solitary
stage) did not discriminate between these volatile
blends. Volatiles from 2-d-infested leaves were preferred to those from 1-d-infested leaves by first
instars, whereas volatiles from leaves infested for
3 d were not attractive to these very young larvae.
Neither were volatiles of leaves infested for 1 d and
then left uninfested for 1 or 2 d attractive to young
larvae. The data suggested that the first and second
instars use volatiles from leaves newly infested by
conspecific larvae as reaggregation cues. We detected
several herbivore-induced compounds in the headspaces of the attractive leaves. Among those, a mixture
of synthetic (E)-b-ocimene, (Z)-b-ocimene, alloocimene, and linalool attracted the larvae (Table 1).
Plant plant volatile information transfer in willows
When HIPVs or volatiles from artificially damaged
plants are received by neighboring conspecific or
Journal of Plant Interactions
heterospecific plants, the receiver plants can become
more resistant to herbivores (Arimura et al. 2009).
This plantplant information transfer has been reported in several plant species (Arimura et al. 2009).
Rhoades (1983) reported that larval growth rates
decreased on undamaged Sitka willows growing near
conspecific trees defoliated by tent caterpillars in the
field. However, the experimental design and interpretation were highly criticized by Fowler and Lawton
(1985). No studies on plantplant signaling in willow
have been reported since. We recently demonstrated
that uninfested willow plants, S. eriocarpa, exposed to
volatiles from conspecifics infested by leaf beetle
adults were more defensive against willow leaf beetle
larvae than those exposed to volatiles from uninfested
conspecifics under both laboratory and field conditions (Yoneya & Takabayashi, 2012). Our data
showed that plantplant volatile information transfer
did exist in willow trees. We will report the details of
our results in forthcoming papers.
Conclusions
The interactioninformation networks of willow
trees, willow leaf beetles, and ladybirds are summarized in Figure 2. In natural communities, multiple
carnivorous species attack P. versicolora. In our
research field, for example, we recorded two unidentified parasitic wasp species that attacked either larval
or adult stages of the leaf beetles. In addition, other
willow species that share a niche with S. eriocarpa in
the wild also attract A. hexaspilota when infested by
P. versicolora, but their signal-based induced indirect
defense differed (Yoneya et al. 2012). Furthermore,
we must consider the fact that signaling between
infested and uninfested willow plants mediated by
HIPVs affected induced direct defense in uninfested
willow plants, modifying the tritrophic interactions.
Thus, interactioninformation networks in natural
willow communities would be more complicated than
shown in Figure 2.
Based on the apparent trade-off between direct
and signal-based induced indirect defense against
willow leaf beetles in willow trees (Yoneya et al.
2012), we hypothesized that willows of a given species
in different communities evolve differently with
respect to signal-based induced indirect defense,
and this might further modify the structure of
interactioninformation networks. To test this
idea, a comparison of direct and indirect defense
traits and multifunctional aspects of plant volatiles
among geographically different willow communities
are needed.
Acknowledgments
This research was financially supported in part by the
Global Center of Excellence Program ‘Formation of a
Strategic Base for Biodiversity and Evolutionary Research:
from Genome to Ecosystem’ of the Ministry of Education,
201
Culture, Sports, Science and Technology (MEXT), Japan,
Core-to-Core project from Japan Science and Technology
Agency, Japan, and by a Grant-in-Aid for Scientific
Research S from the Ministry of Education, Culture,
Sports, Science, and Technology of Japan (No. 19101009).
References
Arimura G, Ozawa R, Shimoda T, Nishioka T, Boland W,
Takabayashi J. 2000. Herbivory-induced volatiles elicit
defence genes in lima bean leaves. Nature. 406:
512515.
Arimura G-i, Matsui K, Takabayashi J. 2009. Chemical
and molecular ecology of herbivore-induced plant
volatiles: proximate factors and their ultimate functions. Plant Cell Physiol. 50:911923.
Baur R, Feeney P, Stadler E. 1993. Oviposition stimulants
for the black swallowtail butterfly identification of
electrophysiologically active compounds in carrot
volatiles. J Chem Ecol. 19:919937.
Choh Y, Shimoda T, Ozawa R, Dicke M, Takabayashi J.
2004. Exposure of lima bean leaves to volatiles from
herbivore-induced conspecific plants results in emission of carnivore attractants: active or passive process?
J Chem Ecol. 30:13051317.
Crowe ML. 1995. Daytime mechanisms of reaggregation in
imported willow leaf beetle, Plagiodera versicolora,
larvae (Coleoptera: Chrysomelidae). Anim Behav.
50:259266.
De Moraes CM, Lewis WJ, Paré PW, Alborn HT,
Tumlinson JH. 1998. Herbivore-infested plants selectively attract parasitoids. Nature. 393:570573.
Du Y, Poppy GM, Powell W, Pickett JA, Wadhams LT,
Woodcock CM. 1998. Identification of semiochemicals
released during aphid feeding that attract parasitoid
Aphidius ervi. J Chem Ecol. 24:13551368.
Engelberth J, Alborn HT, Schmelz EA, Tumlinson JH.
2004. Airborne signals prime plants against insect
herbivore attack. Proc Natl Acad Sci USA.
101:17811785.
Fowler SV, Lawton JH. 1985. Rapidly induced defenses
and talking trees: the devil’s advocate position. Am
Nat. 126:181195.
Guerrieri E, Poppy GM, Powell W, Tremblay E, Pennacchio F. 1999. Induction and systemic release of
herbivore-induced plant volatiles mediating in-flight
orientation of Aphidius ervi. J Chem Ecol. 25:1247
1261.
Hood CE. 1940. Life history and control of the imported
willow leaf beetle. US Dept Agric Circular. 572:19.
Horiuchi J-I, Arimura G-I, Ozawa R, Shimoda T, Takabayashi J, Nishioka T. 2003. A comparison of the
responses of Tetranychus urticae (Acari: Tetranychidae) and Phytoseiulus persimilis (Acari: Phytoseiidae)
to volatiles emitted from lima bean leaves with
different levels of damage made by T. urticae or
Spodoptera exigua (Lepidoptera: Noctuidae). Appl
Entomol Zool. 38:109116.
Kimoto S, Takizawa H. 1994. Leaf beetles (Chrysomelidae)
of Japan. Kanagawa: Tokai University Press. (in
Japanese)
Kimura Y. 1989. Salicaceae. In: Satake Y, Hara H, Watari
S, Tominari, T, editors. Wild flowers of Japan: woody
plants. Tokyo: Heibonsha; p. 3151. (in Japanese)
202
K. Yoneya and J. Takabayashi
Kurosawa Y, Hisamitsu S, Sasaki K. 1985. The color
illustrated book of Japanese beetles (IV). Toyooka:
Hoikusya; p. 323. (in Japanese).
Nakamura M, Miyamoto Y, Ohgushi T. 2003. Gall
initiation enhances the availability of food resources
for herbivorous insects. Funct Ecol. 17:851857.
Raupp MJ, Sadof CS. 1989. Behavioral-responses of a leaf
beetle to injury-related changes in its Salicaceous host.
Oecologia. 80:154157.
Rhoades DF. 1983. Responses of alder and willow to attack
by tent caterpillars and webworms. In: Hedin PA,
editor. Plant resistance to insects, American Chemical
Society Symposium Series 208. Washington DC:
American Chemical Society; p. 5568.
Shiojiri K, Ozawa R, Kugimiya S, Uefune M, Van Wijk M,
Sabelis MW, Takabayashi J. 2010. Herbivore-specific,
density-dependent induction of plant volatiles: honest
or ‘‘cry wolf’’ signals? PLoS One 5:e12161.
Shiojiri K, Takabayashi J, Yano S, Takafuji A. 2002.
Oviposition preferences of herbivores are affected by
tritrophic interaction webs. Ecol Lett. 5:186192.
Takabayashi J, Dicke M. 1996. Plantcarnivore mutualism
through herbivore-induced carnivore attractants.
Trends Plant Sci. 1:109113.
Takabayashi J, Noda T, Takahashi S. 1991. Plants produce
attractants for Apanteles kariyai, a parasitoid of
Pseudaletia separata: cases of ‘‘communication’’ and
‘‘misunderstanding’’ in parasitoidplant interactions.
Appl Entomol Zool. 26:237243.
Takabayashi J, Takahashi S, Dicke M, Posthumus MA.
1995. Developmental stage of herbivore Pseudaletia
separata affects production of herbivore-induced
synomone by corn plants. J Chem Ecol. 21:273287.
Turlings TCJ, Bernasconi M, Bertossa R, Bigler F, Caloz
G, Dorn S. 1998. The induction of volatile emissions in
maize by three herbivore species with different feeding
habits: possible consequences for their natural enemies.
Biol Control. 11:122129.
Wade MJ, Breden F. 1986. Life history of natural populations of the imported willow leaf beetle, Plagiodera
versicolora (Coleoptera, Chrysomelidae). Ann Entomol Soc Am. 79:7379.
Yoneya K, Kugimiya S, Takabayashi J. 2009a. Do adult
leaf beetles (Plagiodera versicolora) discriminate between odors from intact and leaf-beetle-infested willow
shoots? J Plant Interact. 4:125129.
Yoneya K, Kugimiya S, Takabayashi J. 2009b. Can
herbivore-induced plant volatiles inform predatory
insect about the most suitable stage of its prey? Physiol
Entomol. 34:379386.
Yoneya K, Ozawa R, Takabayashi J. 2010. Specialist leaf
beetle larvae use volatiles from willow leaves infested
by conspecifics for reaggregation in a tree. J Chem
Ecol. 36:671679.
Yoneya K, Takabayashi J. 2012. Does plantplant
signalling affect the colonization and diversity of
arthropods on willow plants? Poster session presented
at: Joint meeting of the 59th annual meeting of ESJ and
the 5th EAFES international congress; Otsu, Japan.
Yoneya K, Uefune M, Takabayashi J. 2012. An apparent
trade-off between direct and signal-based induced
indirect defence against herbivores in willow trees.
PLoS One 7:e51505.