Phytochemistry: Monika Hilker, Torsten Meiners

Phytochemistry 72 (2011) 16121623
Contents lists available at ScienceDirect
Phytochemistry
journal homepage: www.elsevier.com/locate/phytochem
Review
Plants and insect eggs: How do they affect each other?

Monika Hilker , Torsten Meiners
Freie Universitt Berlin, Institute of Biology, Applied Zoology/Animal Ecology, Haderslebener Str. 9, D-12163 Berlin, Germany
a r t i c l e
i n f o
Article history:
Available online 23 March 2011
Keywords:
Plant volatiles
Plant surface
Plant boundary layer
Plant defence
Oviposition-induced defence
Herbivorous insect
Insect oviposition
Elicitor
Oviposition-induced transcription
a b s t r a c t
Plantinsect interactions are not just inuenced by interactions between plants and the actively feeding
stages, but also by the close relationships between plants and insect eggs. Here, we review both effects
of plants on insect eggs and, vice versa, effects of eggs on plants. We consider the inuence of plants on
the production of insect eggs and address the role of phytochemicals for the biosynthesis and release of
insect sex pheromones, as well as for insect fecundity. Effects of plants on insect oviposition by contact
and olfactory plant cues are summarised. In addition, we consider how the leaf boundary layer inuences
both insect egg deposition behaviour and development of the embryo inside the egg. The effects of eggs on
plants involve egg-induced changes of photosynthetic activity and of the plants secondary metabolism.
Except for gall-inducing insects, egg-induced changes of phytochemistry were so far found to be detrimental to the eggs. Egg deposition can induce hypersensitive-like plant response, formation of neoplasms or
production of ovicidal plant substances; these plant responses directly harm the eggs. In addition, egg
deposition can induce a change of the plants odour and leaf surface chemistry which serve indirect plant
defence with the help of antagonists of the insect eggs. These egg-induced changes lead to attraction of egg
parasitoids and their arrestance on a leaf, respectively. Finally, we summarise knowledge of the elicitors of
egg-induced plant changes and address egg-induced effects on the plants transcriptional pattern.
2011 Elsevier Ltd. All rights reserved.
Contents
1.
2.
3.
4.
5.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Plant effects on insect eggs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.1.
Plant chemistry affects insect mating and production of eggs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.2.
Plant chemical cues affect oviposition behaviour of herbivorous insects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
2.3.
Plant chemistry influences quality of insect eggs and embryo development . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Egg effects on plants . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.1.
Insect egg deposition affects the plants primary metabolism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.2.
Insect egg deposition changes the plants secondary metabolism . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.2.1.
Egg deposition affects plant volatile emission . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.2.2.
Egg deposition affects plant surface chemistry. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
3.2.3.
Egg deposition affects biosynthesis of non-volatile plant internal secondary metabolites . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Interacting factors of plants and insect eggs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.1.
Egg-associated secretions elicit plant responses . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
4.2.
Phytohormones and plant defence genes respond to eggs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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1. Introduction
Abbreviations: BA, benzoic acid; CHC, cuticular hydrocarbon; HR, hypersensitive
response; IG, iridoid glycoside; JA, jasmonic acid; PA, pyrrolizidine alkaloid; SA,
salicylic acid; TPS, terpene synthase.
Corresponding author. Tel.: +49 30 8385 5913; fax: +49 30 8385 3897.
E-mail address: hilker@zedat.fu-berlin.de (M. Hilker).
0031-9422/$ - see front matter 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.phytochem.2011.02.018
Plants serve as oviposition sites for most herbivorous insects

which deposit their eggs on almost all parts of the plants. For
example, the sunower stem weevil Cylindrocopturus adspersus
M. Hilker, T. Meiners / Phytochemistry 72 (2011) 16121623
(LeConte) or the Viburnum L. leaf beetle Pyrrhalta luteola (Mller)

deposit eggs on stems; nitidulid pollen beetles and many fructivorous insects use the reproductive parts, the owers and fruits, as
oviposition sites. The majority of herbivorous insect species including herbivorous hemipteran, lepidopteran, coleopteran and hymenopteran species oviposit on leaves. Only few herbivorous insects
lay their eggs in the soil in the vicinity of plants, as e.g. many
Orthoptera or insects with root-feeding larvae.
Egg deposition by herbivorous insects is the start of the establishment of a new herbivore generation. From the plants perspective, strategies are benecial which prevent herbivores from egg
deposition on the plant, which reduce the number of eggs laid or
which impair the development of the embryo inside the eggs. From
the herbivores perspective, tness is maximised when behavioural
responses to plant cues lead to oviposition on plants where progeny will nd suitable food.
In this review, we consider plant effects on egg-laying herbivorous insects and their eggs (Section 2). Even though herbivorous
insects are well adapted to plant cues and can efciently exploit
them for successful reproduction, plants are no defenceless victims
of egg-laying insects. They may deter egg deposition and inuence
the development of the herbivores embryo. We address in this review how plants change their primary and secondary metabolism
in response to insect eggs (Section 3). The egg-induced changes of
plant secondary metabolites, especially of plant volatile terpenoids, have been shown to serve a protective role against herbivore
attack. Furthermore, we review the knowledge of the mechanisms
of plantegg interactions (Section 4).
1613
2. Plant effects on insect eggs

The various effects of plants on insect eggs are outlined in Fig. 1.
Production of fertile eggs requires successful mating in non-parthenogenously reproducing herbivorous insects. Biosynthesis and
release of mating signals as well as production of eggs may be
inuenced or even determined by plant chemicals. Odour of plants,
the plant surface and the plants interior (Stdler, 2002) guide
egg-laying herbivorous insect females to their host plants and
inuence the choice of oviposition sites. The eggs may benet from
plant toxins sequestered by their parents from food, as the toxins
may deter egg predators and parasitoids (reviewed by Blum and
Hilker, 2002). Since eggs laid on a leaf are enclosed by the leafs
boundary layer (see Section 2.3), the concentration of leaf volatiles
and atmospheric gases in this layer may specically affect embryonic development. Below we will address these aspects of plant effects on insect eggs.
2.1. Plant chemistry affects insect mating and production of eggs
In many insect species, plant secondary metabolites provide
essential direct precursors for the biosynthesis of sex pheromones
which mediate successful mating. One of the most famous examples is the sequestration of plant pyrrolizidine alkaloids (PAs) by
larvae of arctiid moths; the plant alkaloids are maintained through
all arctiid life stages as non-toxic N-oxides. Males of several arctiid
species can convert the plant PAs to hydroxydanaidal and release it
as courtship pheromone from their coremata (Hartmann et al.,
Fig. 1. Effects of phytochemicals on insect mating and reproduction, oviposition, egg development and protection of eggs. For details, see text Section 2.
1614
2004). Besides lepidopteran species, other well known examples of

use of plant secondary metabolites for herbivore pheromone biosynthesis are tephritid ies (Bactrocera spp. Macquart) which
sequester methyl eugenol from their host plants. Eugenol derivatives are accumulated in the rectal glands of adult males (Shelly
and Nishida, 2004) and serve as male sex pheromones (Hee and
Tan, 2004, 2006). Not only plant secondary metabolites, but also
the fatty acid pattern of a plant can determine the blend of insect
cuticular hydrocarbons (CHCs) that may serve as mate recognition
cues. For example, the CHC prole of the mustard leaf beetle, Phaedon cochleariae (F.) is signicantly inuenced by the host plant species the beetle is feeding upon (Geiselhardt et al., 2009). Male P.
cochleariae of two laboratory lines that were fed with different host
plants (Chinese cabbage, watercress) preferred to mate same host
plant females to different host plant females and also attempted
to mate more often glass dummies treated with CHC extract of females of the preferred line (Geiselhardt, Otte, Hilker, unpublished
data). Hence, plant chemistry may inuence success of mating of
herbivorous insects, and thus, production of their progeny.
Some herbivorous insects are known to adjust their production
and release of sex pheromones to the presence of plant volatiles
which indicate suitable food for the progeny (Landolt and Phillips,
1997; Reddy and Guerrero, 2004). For example, volatiles from corn
silk or tomatoes, especially ethylene, 3-methyl-butan-1-ol, phenylacetaldehyde, trigger sex pheromone production in the abdominal
glands of female Helicoverpa spp. Hardwick whose larvae feed on
fruiting parts of various plants (Raina et al., 1992). The presence
of plant volatiles can not only affect the pheromone signaller, but
also the receiver. Plant volatiles may function as sexual kairomones (Ruther et al., 2002) and enhance the attractiveness of insect sex pheromones (Deng et al., 2004; Dickens, 1989; Light
et al., 1993). For example, green leaf alcohols attract swarming
cockchafer males (Melolontha spp. F.) to sites where conspecic females which emerged earlier after overwintering are already feeding on a plant; the sex pheromones released by Melolontha F.
females (1,4 benzoquinone, toluquinone) are only slightly attractive or even non-alluring; however, they synergize the attractiveness of feeding-induced green leaf alcohols (Reinecke et al.,
2002; Ruther et al., 2000). Studies on the mechanism of effects of
plant volatiles on responses to insect pheromones revealed that
plant volatiles affect the ring of pheromone olfactory receptor
neurons in dependence of the ratio of pheromone and plant volatile compound and of the temporal pattern at which pheromone
and plant volatiles are experienced by the insect (e.g. Party et al.,
2009, and references therein).
Plant chemistry does not only affect mating signals and thus,
reproductive success of herbivorous insects, but more directly also
the production of eggs, i.e. oogenesis. Females need to provide the
developing eggs with nutritive substances to ensure successful
development of the embryo. The nutrients are provided by the
plant the female is feeding upon. High plant nutritional quality is
usually associated with production of a high number of eggs.
Low plant nutritional quality is usually linked with less active
oogenesis. However, the eggs produced by females feeding on a
low-quality plant may be larger than those from females feeding
on a high-quality plant. Fox and Czesak (2000) review the models
on optimal progeny size that suggest a trade-off between progeny
size and number. Larger eggs are supposed to release larger larvae
which might have a developmental advantage on poor-quality
plants compared to smaller larvae (Ekbom and Popov, 2004).
2.2. Plant chemical cues affect oviposition behaviour of herbivorous
insects
Erich Stdler (2002) eminently reviewed studies on the impact
of plant chemical cues important for egg deposition by herbivorous
insects. He outlined the importance of both plant surface compounds as well as of the chemistry of the plant interior for the
choice of oviposition sites and addressed the question how herbivorous insects decipher the complex information on plant quality
obtained by olfactory and contact perception of both oviposition
stimulants and deterrents. Stdler raised the question how an
egg-laying female that does not wound the plant surface can perceive oviposition-stimulating plant chemicals mainly present inside the plant cell. For example, oviposition by butteries
specialised on brassicaceous plants (e.g. Pieris spp. Schrank) is
stimulated by secondary plant compounds typical for this taxon,
the glucosinolates (Stdler and Reifenrath, 2009). However, these
glucosinolates are present mainly inside the plant cell (Reifenrath
et al., 2005). Prior to egg deposition, some butteries specialised on
Brassicaceae drum with their forelegs on host plant leaves. This
drumming behaviour may be crucial to scratch the leaf surface
and gain access and contact to the oviposition stimulants underneath the outermost wax layer.
In addition to plant chemicals that affect insect oviposition
upon contact, plant volatiles released from both owers and vegetative parts play a crucial role in guiding oviposition behaviour of
gravid insect females (e.g. Reisenman et al., 2009, 2010).
For pollination, ower volatiles attract nectar-feeding adult
Lepidoptera which do not only serve pollination, but also oviposit
on the plant and thus threaten it by their herbivorous larval progeny. Hence, these plants face the dilemma of attracting pollinators
(as mutualists), but avoiding larval herbivory by the same pollinators progeny (as antagonists). Some solanaceous plants address
this problem by attracting the nocturnal hawkmoth Manduca sexta
L. by ower volatiles for pollination when undamaged, but reduce
their attractiveness to adults by change of the oral odour when
damaged by hawkmoth larvae (Kessler et al., 2010). Flowering,
undamaged tobacco plants attract M. sexta by benzyl acetone;
when plants are damaged by moth larvae, they release less of the
attractive volatile. Furthermore, feeding damaged tobacco plants
can reduce the percentage of owers opening during night. Compared to undamaged plants, tobacco plants with feeding damage
show more open owers in the morning when the hawkmoths
are no longer active, but hummingbirds are attracted for pollination. This shift in phenology prevents further moth oviposition
(Kessler et al., 2010). Hence, the plants become pollinated at the
cost of some feeding damage that can be limited by reducing the
release of ower volatiles and changing ower opening activity
in response to damage.
Constitutive volatiles of the vegetative parts of a host plant may
attract gravid insect females, whereas volatiles from a feedingdamaged plant may act as repellent. Plants show a high plasticity
in volatile emission, and herbivores often respond to plant volatiles
depending on the plants infestation status. Avoiding feedinginduced plant volatiles may be considered an adaptation of herbivores to prevent competition since feeding-induced volatiles signalise infestation by conspecics (De Moraes et al., 2001). For
example, females of the elm leaf beetle Xanthogaleruca luteola Mller avoid competition among their progeny by orienting to odours
from plants with few eggs and low feeding damage rather than to
odours from highly infested plants with a high egg load and high
feeding damage (Meiners et al., 2005). In addition to induced host
plant volatiles, also constitutively released volatiles from non-host
plants can affect oviposition behaviour of both herbivorous insects
and their parasitic wasps. Such non-host plants are often used for
intercropping with host plants in order to manipulate herbivore
behaviour for pest control (Cook et al., 2007).
While plant volatiles can repel or attract a gravid female from a
distance and non-volatile plant cues can deter or stimulate oviposition upon contact, the chemicals of the so-called leaf boundary
layer may also be important for choice of oviposition sites.
Humidity, concentrations of oxygen and carbon dioxide as well as

of other volatiles released from the plant may be different in the
boundary layer and the headspace above the plant (Schuepp,
1993). The boundary layer thickness varies with the wind speed
and leaf dimension and is estimated to range between 1 and
5 mm. Thus, a small insect egg is usually embedded in the
boundary layer (Woods, 2010).
Ovipositing insects might use gas concentrations in the boundary layer for their nal choice of an oviposition site (Stdler, 1986).
For example, photosynthetically highly active plants that x large
amounts of CO2 are expected to show a CO2 gradient between leaf
surface, boundary layer and atmosphere above the boundary layer.
This gradient might be used by insects to detect photosynthetically
highly active and thus possibly highly nutritive plants (Langan
et al., 2001). Female cactus moths, Cactoblastis cactorum Berg, actively probe the plant surface prior to oviposition with their CO2sensors. This behaviour might enable the moth to detect the
healthiest, most active plant (parts) (Stange, 1997; Stange et al.,
1995). The importance of CO2 concentrations around a plant has
also been shown for M. sexta. The nectar-feeding moth prefers surrogate owers that emit CO2 levels characteristic of a owering
plant (Thom et al., 2004).
2.3. Plant chemistry inuences quality of insect eggs and embryo
development
The humidity and gas concentrations in the boundary layer of a
leaf may signicantly affect egg development (Woods, 2010). High
concentrations of compounds such as volatile plant terpenes could
enter the eggs via the aeropyles in the outermost layer, the proteinaceous chorion, diffuse through the next layer, i.e. the wax layer,
and thus reach the embryo behind the vitelline envelope and serosa. Low humidity due to dry air and closed plant stomata may
lead to desiccation of the eggs. A plant may respond to insect eggs
by hypersensitive response, i.e. formation of necrotic tissue at the
site of egg deposition (see also Section 3.2.2: Balbyshev and
Lorenzen, 1997; Little et al., 2007; Shapiro and DeVay, 1987). At
such a necrotic site, humidity decreases and local temperature
increases. The metabolic rate of the embryo will increase because
of the increase of leaf temperature, but also water loss of the egg
will increase. As a result, the egg will probably desiccate and the
stressed embryo will die (Woods, 2010).
In addition to the immediate gas atmosphere provided by the
leaf boundary layer enclosing an insect egg, performance of eggs
may also be affected by plant secondary compounds incorporated
into the eggs by the females sequestering those compounds from
the plant. The secondary plant compounds often serve as protection from parasitisation and predation of eggs (Blum and Hilker,
2002). For example, chrysomelid beetles of the taxon Diabroticina
sequester bitter cucurbitacins from their host plants and transfer
them to the eggs (Ferguson et al., 1985). Some willow leaf beetles
include the bitter tasting salicin from willows and poplars into
their eggs (Pasteels et al., 1986). Numerous lepidopteran species
are known to endow their eggs with plant toxins, e.g. aristolochic
acids from Aristolochia L. plants in the eggs of the papilionid Atrophaneura alcinous (Klug) (Nishida and Fukami, 1989), cardenolides
from milkweeds, Asclepias L. spp., in the eggs of the monarch buttery (Roeske et al., 1976), and N-oxidised alkaloids in the eggs of
several Lepidoptera (arctiids, nymphalids), Chrysomelidae and
Hemiptera that feed on plants containing PAs (Boppr, 1990;
Hartmann, 1995a,b, 1999; Loaiza et al., 2007; Schaffner et al.,
1994; Trigo et al., 1996). Adults of Naupactus bipes (Germar)
(Curculionidae) feeding on Piper gaudichaudianum Kunth
(Piperaceae) sequester chromenes from the leaves, and females
incorporate them in the eggs (Ramos et al., 2009). Not only the
females endow the eggs with plant toxins, but also the males can
1615
contribute to the endowment of eggs with plant toxins; males

transfer the toxins to the eggs via mating (Eisner et al., 2002, and
references therein).
In addition to such plant toxins, the phytohormones jasmonic
acid (JA) and salicylic acid (SA), as well as a precursor of SA, benzoic
acid (BA), have been detected in eggs of many insect species, often
in much higher concentrations than in plant tissue or larval diet
(Tooker and de Moraes, 2005, 2007). The function of these compounds in insect eggs is unknown. SA and BA have antimicrobial
and antifungal activity and thus, might protect eggs from entomopathogens. JA, SA and BA have been detected so far only inside the
eggs. However, they were not found in extracts of the exterior of
eggs (Tooker and De Moraes, 2005). Even though it is tempting
to assume a role of these endogenous compounds of the eggs in
triggering egg-induced plant defence, such a role is questionable
at the current state of knowledge.
3. Egg effects on plants
The interaction between plants and insect eggs is not unidirectional. While plants can inuence mating activities and oviposition
behaviour of herbivorous insects, the eggs themselves when laid
on the plant can change the plants primary and secondary metabolism. So far, these egg-induced effects on plants have been shown
mainly detrimental to eggs. Hence, the egg-induced effects are
considered plant defensive responses against egg deposition by
herbivorous insects. Nevertheless, insect eggs can also trigger plant
responses which are benecial for the eggs or the hatching larvae,
as is the case in some insect species inducing plant galls. Some insects induce the formation of a plant gall by egg deposition rather
than by larval feeding; the gall provides shelter for the egg and
nutritive tissue to the hatching larva. Oviposition-induced effects
on a plant by galling insects have been reviewed by Hilker et al.
(2002b) and will not be considered here.
One might expect especially short-lived, small crop plants with
low biomass to show oviposition-induced defence, as these plants
might especially benet from prevention or reduction of feeding
damage by larvae that will hatch from the eggs. However, defence
induced by insect eggs is known in both trees with their huge biomass and long life and short-lived, small crop plants. Hence, plants
with very different life strategies evolved mechanisms to respond
to herbivorous insects at such an early stage of attack, the egg
deposition. The parallels and differences of the plantinsect systems studied with respect to egg-induced plant effects are summarised in Table 1 and will be addressed below.
3.1. Insect egg deposition affects the plants primary metabolism
Egg deposition by chewing and sucking herbivorous insects can
lead to a reduction of the plants photosynthetic activity both locally, i.e. directly at the leaves with eggs, and systemically, i.e. at
leaves adjacent to those with eggs. A systemic reduction of the
net photosynthetic rate was found in egg-free twigs of Scots pine
(Pinus sylvestris L.) adjacent to twigs laden with eggs of the herbivorous pine sawy Diprion pini L. (Schroeder et al., 2005). Local photosynthetic activity was measured in Brassica oleracea L. (savoy
cabbage) leaves laden with eggs by the herbivorous harlequin
bug Murgantia histrionica (Hahn) (Velikova et al., 2010); in this
study, measurements of photosynthetic activity were made directly at the leaf with eggs, but at parts of the leaf with access to
light and not covered by eggs. Since oviposition by M. histrionica
is usually associated with feeding by the females on the leaves,
the authors also measured the effect of feeding on the plants photosynthetic activity and found that feeding reduces the plants photosynthetic activity. Moreover, plants which experienced both
feeding damage and egg deposition by this bug show signicantly
1616
Table 1
Overview of changes of plant primary and secondary metabolism caused by insect egg deposition. For details, see text Section 3.
Effect of insect egg deposition
On plant primary metabolism
Reduction of photosynthetic activity
Reduction of photosynthetic activity
Reduction of transcription of
photosynthesis-relevant genes
No change of net photosynthetic rate
Plant
Herbivorous Insect
References
Scots pine, Pinus sylvestris

Savoy cabbage, Brassica
oleracea
Thale cress, Arabidopsis
thaliana
Field elm, Ulmus minor
Pine sawy, Diprion pini

Harlequin bug, Murgantia
histrionica
Cabbage buttery, Pieris brassicae
Schroeder et al. (2005)

Velikova et al. (2010)
Elm leaf beetle, Xanthogaleruca

luteola
Meiners (unpublished data)
Elm leaf beetle, Xanthogaleruca

luteola
Pine sawy, Diprion pini
Southern green stink bug, Nezara
viridula
Southern green stink bug, Nezara
viridula
Harlequin bug, Murgantia
histrionica
Meiners and Hilker (2000), Wegener et al. (2001)

and Bchel et al. (unpublished data)
Mumm et al. (2003)
Colazza et al. (2004a,b)
Spotted stemborer moth, Chilo

partellus
Bruce et al. (2010)

Fatouros et al. (2005)

Hilker, Blenn, Geiselhardt, Fatouros, unpublished
data
Colorado potato leaf beetle,

Leptinotarsa decemlineata
Cabbage butteries, Pieris
brassicae, P. rapae
Balbyshev and Lorenzen (1997)
On plant secondary metabolism

(a) Induction of plant volatiles: attractive to egg parasitoids
Terpenoids
Field elm, Ulmus minor
(E)-b-Farnesene
(E)-b-Caryophyllene
(E)-b-Caryophyllene
Scots pine, Pinus sylvestris

French bean, Phaseolus
vulgaris
Broad bean, Vicia faba
(E)-b-Caryophyllene
Savoy cabbage, Brassica

oleracea var. sabauda
(b) Change of plant odour: attractive to larval parasitoids
Reduced emission of (Z)-3-hexenyl
Palisade signal grass,
acetate
Brachiaria brizantha
(c) Induction of change of plant surface chemistry
Brussels sprouts, Brassica
Changes of the quantitative
oleracea var. gemmifera
composition of leaf surface
compounds
thaliana
Necrotic zones
Hybrid of Solanum spp.
Necrotic zones
Mustard, Brassica nigra
Accumulation of callose; production

of H2O2
Neoplasma formation

thaliana
Pea, Pisum sativum
(d) Induction of non-volatile plant secondary metabolites

Production of benzyl benzoate
Rice, Oryza sativa
(ovicidal activity)
Little et al. (2007)
Colazza et al. (2004a,b)

Conti et al. (2008)
Shapiro and DeVay (1987)

Little et al. (2007)
Bruchid beetles, Bruchus pisorum;

Callosobruchus maculatus
Doss et al. (2000)
White-backed planthopper,
Sogatella furcifera
Seino et al., 1996; Suzuki et al., 1996
lower photosynthetic activity than plants which are egg-free, but

suffered feeding damage. These ndings demonstrate that egg
deposition per se may signicantly affect the plants primary
metabolism and reduce photosynthetic activity both in a tree species (pine) and a crop plant (savoy cabbage).
Whether transcription of genes involved in photosynthesis is affected locally at the leaf with eggs but next to the oviposition site,
or systemically at egg-free leaves adjacent to the egg-laden ones
has not been studied so far. In Arabidopsis thaliana (L.), transcription of genes involved in photosynthesis was measured directly
at the site where Pieris brassicae (L.) had laid an egg mass; the
authors removed the egg mass 1, 2 or 3 days after egg deposition
and found that transcript levels of photosynthesis-relevant genes
in the tissue where the eggs have been laid are reduced at each
time interval (Little et al., 2007). Since leaf parts covered with eggs
have no or reduced access to light, the transcriptional reduction
found in this study of A. thaliana with buttery eggs may be due
to this shadowing effect rather than to specically egg-induced effects. Thus, while transcription of photosynthesis-related genes in
tissue right below the eggs is changed perhaps due to the shadowing effect of eggs, we do not know yet how eggs affect transcription
in tissue not shadowed by the eggs, but adjacent to them (compare
local and systemic effects described above). Hence, the mechanisms of egg-induced effects in tissue adjacent to the oviposition
site are unknown so far.
While only few studies are available that studied the effect of
insect egg deposition on photosynthetic activity, numerous studies addressed the impact of insect feeding damage on photosynthesis (e.g. Nabity et al., 2009; Welter, 1989; Zangerl et al.,
2002). The effect of feeding damage on photosynthetic activity

depends on a wide range of factors such as the plant and herbivore species, the type of feeding damage (sucking, mining, or
chewing herbivores), or the site of measurement (damaged
leaves or undamaged leaves of a damaged plant, or the canopy)
(Delaney, 2008, and references therein). Partial plant damage
was found to cause an increase, no change, or decrease of the
net photosynthesis locally at the site of damage and systemically
at adjacent undamaged leaves. Interestingly, systemically reduced photosynthesis as it was found after egg deposition on
pine (Schroeder et al., 2005), is very rare after feeding damage
(Delaney, 2008).
Does the plant benet from reduction of photosynthetic activity
in egg-laden leaves and adjacent ones? High photosynthetic activity rather than reduced one might be expected in egg-laden leaves
to cover current costs of plant defence against eggs and to compensate in time for upcoming larval feeding damage (see Section 3.2).
Compensation of plant damage by enhanced photosynthesis is
considered a trait of plant tolerance towards herbivory (Herms
and Mattson, 1992; Karban and Baldwin, 1997). Hence, the reduction of photosynthesis induced by insect egg deposition on pine
and savoy cabbage indicates that defence against eggs is costly
for these plant species and might be paid by reduced tolerance to
upcoming herbivory (Schroeder et al., 2005). However, the expenses of egg-induced plant defence and the possibly negative effects of egg-induced reduction of photosynthesis might be limited
by the fact that the time between egg deposition and larval hatching is usually only a few days (except for eggs overwintering on a
plant).
3.2. Insect egg deposition changes the plants secondary metabolism

3.2.1. Egg deposition affects plant volatile emission
Egg deposition by herbivorous insects can induce a change of
the plants volatile blend. The oviposition-induced plant volatiles
were shown to attract egg parasitoids killing the eggs of the herbivores. Mainly oviposition-induced emission of terpenoids was
found to play a role in parasitoid attraction.
The rst study which demonstrated that insect egg deposition
induces a change of plant volatile emission locally at the site of
egg deposition and systemically was a study of elm (Ulmus minor
Mill.) laden with eggs of the elm leaf beetle X. luteola (Meiners
and Hilker, 2000). Odour from elm leaves laden with eggs was
shown to attract a parasitoid species specialised on elm leaf beetle
eggs. The parasitoid responds specically only to volatiles emitted
after elm leaf beetle egg deposition, whereas odour of leaves with
eggs laid by other herbivorous insects does not attract this specialised parasitoid Oomyzus galerucivorus (Hedqvits), a eulophid wasp
(Meiners et al., 2000). Hence, the attractiveness of elm leaves with
eggs towards this specialised egg parasitoid is specic for the herbivore species. Odour of elm leaves becomes attractive to egg parasitoids a few hours after elm leaf egg deposition and keeps
attractiveness for about 5 days, i.e. shortly before larvae hatch
(Meiners, unpublished data).
These results on the attractiveness of odour from elm leaves laden with elm leaf beetle eggs triggered several questions, i.e.
Do the eggs indeed induce the attractive plant volatiles or does
the ovipositional wounding associated with egg deposition
induce the attractants? The elm leaf beetle female is removing
the leaf epidermis with her mouthparts prior to egg deposition.
Do egg-free leaves that experienced regular feeding activity also
emit volatiles that attract the egg parasitoid? Regular feeding
activity is visible by holes chewed into a leaf and is usually
accompanied by beetle egg deposition.
Does a combination of odour released from eggs per se and from
feeding-damaged sites cause attraction of the parasitoid rather
than an induction of plant volatiles by egg deposition?
These questions may be considered a general guide which enables to distinguish between egg-induced effects and woundingor feeding-induced ones, when studying plant responses to egg
deposition by insects which feed prior to egg laying.
The studies of these questions in the tritrophic system consisting of elm, elm leaf beetle and egg parasitoid showed that ovipositional leaf damage (epidermal removal) does not induce the
volatiles attractive to the parasitoid of leaf beetle eggs. Neither
do volatiles from egg-free leaves that have been damaged by feeding activity of elm leaf beetles attract the parasitic wasp, whereas
leaves with eggs and feeding damage are attractive to the parasitoid. In order to prove that attraction of the egg parasitoid is indeed
due to induction of plant volatiles by oviposition rather than to a
combination of odour released from feeding-damaged leaves and
from egg odour, the parasitoids behavioural response was tested
to a mixture of odour from feeding-damaged leaves (without eggs)
and from eggs that were removed from a leaf. The odour mixture
does not attract the parasitoid; this study demonstrated that the
attraction of the egg parasitoid is indeed due to an inductive effect
of elm leaf beetle egg deposition on the plants volatile pattern
(Meiners and Hilker, 2000).
The volatile blend of locally and systemically ovipositioninduced elm leaves with feeding damage contains mainly green
leaf volatiles and terpenoids (Wegener et al., 2001). Inhibition of
terpenoid biosynthesis in elm leaves with eggs and feeding damage by treatment of elm with terpenoid biosynthesis inhibitors
(fosmidomycin and cerivastatin) leads to a loss of the plants
1617
attractiveness to the parasitoid (Bchel, Malskies, Mayer, Fenning,

Gershenzon, Hilker, Meiners, unpublished data). These ndings
show the importance of induction of terpenoids necessary for
attraction of the parasitoid of elm leaf beetle eggs.
Another tree, i.e. Scots pine (P. sylvestris) was also shown to
respond specically to egg deposition by herbivorous insects.
When pine sawies like D. pini and Neodiprion sertifer (Geoffroy)
slit pine needles longitudinally to insert a row of eggs into the
needle, the pine twig laden with eggs starts to change its odour
locally and systemically 3 days after oviposition. The odour released after egg deposition attracts egg parasitoids specialised
on eggs of these diprionids. In contrast, odour of egg-free pine
needles which were slit by a needle to mimic the ovipositional
wounding is not attractive to the egg parasitoid (Hilker et al.,
2002a). However, pine foliage releases attractive odour when
secretion associated with the eggs was applied into an articially
slit pine needle (Hilker et al., 2005). Thus, wounding per se does
not induce the change of pine odour, but egg deposition or egg
secretion applied to the ovipositional wound does. Adult sawies
do not feed upon pine needle tissue. Odour of pine which suffered larval feeding damage is not attractive to the egg parasitoid
(Hilker, unpublished data).
A series of bioassays showed that only pine odour released
3 days after sawy egg deposition is attractive, whereas odour released earlier or later than 3 days has no behavioural effect on the
parasitoid (Hilker et al., 2002a; Koepke et al., 2010; Schroeder
et al., 2008). In 4-day-old eggs, the diprionid embryo might have
developed so far that the parasitoid larva inside the host egg is
probably not able to develop successfully next to a host embryo
of this age; thus, pine with 4-day-old diprionid eggs will probably
not benet from attraction of egg parasitoids by oviposition-induced pine volatiles. Pine twigs with diprionid eggs might afford
the time-limited release of oviposition-induced plant volatiles
since egg parasitoids are attracted by the sex pheromones of diprionid females (Hilker et al., 2000); these pheromones (acetate and
propionate of (2S,3R,7R)-3,7-dimethyl-2-tridecanol) will attract
the parasitoid to freshly laid eggs whereas the oviposition-induced
plant odour probably becomes important when no or too low concentrations of sex pheromones are around 3 days later. Hence, release of oviposition-induced plant volatiles during only a narrow
time window (i.e. 3 days after egg deposition) may be considered
a very economic and efcient way of the plant to call parasitoids
for help (Dicke and Baldwin, 2010).
The attractive oviposition-induced pine odour differs from
unattractive odour released from egg-free, slit pine needles by its
quantitative composition; no qualitative differences are detectable
(Mumm et al., 2003). The attractive odour contains signicantly
greater amounts of (E)-b-farnesene. This sesquiterpene is not
attractive per se to the parasitoid at neither concentration tested
(Mumm and Hilker, 2005). However, when (E)-b-farnesene is combined with the habitat (background) odour of non-induced pine,
the egg parasitoid responds positively and is attracted. These ndings show that the oviposition-induced key compound needs to be
perceived in a natural odorous context to elicit a behavioural response in the parasitoid (Beyaert et al., 2010).
In addition to these tree species, changes of plant volatiles after
insect egg deposition have been shown in several crop plants, i.e.
in French bean Phaseolus vulgaris L. and broad bean Vicia faba L.
after egg deposition by the herbivorous pentatomid bug Nezara
viridula L. (Colazza et al., 2004a,b),
in savoy cabbage B. oleracea L. var. sabauda after egg deposition
by the pentatomid M. histrionica (Conti et al., 2008), and
in palisade signal grass Brachiaria brizantha Stapf after egg
deposition by the stemborer moth Chilo partellus (Swinhoe)
(Bruce et al., 2010).
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The oviposition-induced effects on bean and cabbage show

many parallels to those described above for trees; thus, both plants
with a relatively short lifetime and those which grow for decades
and have plenty of time to regrow after feeding damage respond
to the very early phase of insect attack, the egg deposition, in a
similar way. Like in elm and pine, bean plants with eggs of N. viridula emit the odour attractive to egg parasitoids only during a specic time window after egg deposition. Bean plants with about 4
5-day-old eggs do no longer emit odour attractive to parasitoids
(Colazza et al., 2004a). Like in the elm leaf beetle, egg deposition
by N. viridula is associated with feeding activity of the adults (here:
piercing-sucking activity). In contrast to egg deposition by the elm
leaf beetle and the dipriond sawies mentioned above, no ovipositional wounding of the leaf occurs when N. viridula lays eggs; the
eggs are just glued on the plant cuticle. Like in the tree studies outlined above, the volatiles released from bean plants after feeding
damage by bugs do not attract egg parasitoids. Again, the oviposition-induced odour of bean plants is characterised by terpenoids,
i.e. here by increased amounts of (E)-b-caryophyllene when compared to non-attractive plants. Also the cabbage plants with feeding damage and egg deposition by M. histrionica release increased
amounts of (E)-b-caryophyllene when compared to non-attractive,
undamaged plants (Conti et al., 2008). Hence, oviposition-induced
plant terpenoids play a crucial role in both trees and the dicotylenous crops studied so far for indirect plant defence against eggs.
In contrast, the change of plant odour after egg deposition by
the stemborer C. partellus on palisade signal grass is not characterised by increased release of terpenoid volatiles, but a signicant
decrease of the emission of (Z)-3-hexenyl acetate. Female C. partellus moths preferred plants without eggs to plants with eggs. Odour
released from egg-laden palisade signal grass B. brizantha caused
increased attraction of the larval parasitoid Cotesia sesamiae (Cameron) when compared to odour of egg-free, undamaged plants
(Bruce et al., 2010). Hence, changes of plant odour after insect
egg deposition are not only exploited by egg parasitoids, but can
also alert larval parasitoids and provide information on upcoming
availability of host larvae.
Like many other lepidopteran species, females of the moth C.
partellus do not damage the plant when laying eggs. Nevertheless,
some lepidopteran species move their ovipositor back and forth on
the leaf surface or drum with their legs on the substrate prior to
oviposition (Stdler, 2002). Many lepidopteran species leave hairs
and scales at the site of egg deposition which may have kairomonal
function for egg parasitoids (Fatouros et al., 2008a,b).
Hence, in order to distinguish egg-induced changes of plant
metabolism from effects caused by drumming and scratching
behaviour of the female or by the release of scales and hairs, one
should address the following questions when studying plant responses to egg deposition by insects which do not feed upon the
plant prior to egg laying, as is the case for lepidopteran species:
Do just eggs or egg-associated secretions (see Section 4.1) really
induce plant responses or
Does scratching the leaf surface or drumming induce plant
changes?
Do scales and hairs left by egg-laying females on leaves induce
plant changes, or do they effectively absorb plant volatiles by
enlarging the absorptive surface?
Are there combinatory effects of eggs and female scales and
hairs, respectively?
3.2.2. Egg deposition affects plant surface chemistry

Specic plant traits like a thick waxy plant cuticle may impair
release of oviposition-induced plant volatiles when obvious damage of tissue is lacking. Furthermore, change of plant odour in such
a way that it becomes attractive to egg parasitoids might be impossible in leaves that hardly produce terpenoids which seem to be
important for attraction of egg parasitoids. Egg deposition by P.
brassicae on the waxy leaves of Brussels sprouts (B. oleracea L.
var. gemmifera) does not induce volatiles that attract the egg parasitoid Trichogramma brassicae (Fatouros et al., 2005). Nor does egg
deposition by P. brassicae on leaves of A. thaliana lead to emission
of odour that attracts the egg parasitoid T. brassicae (Hilker, Blenn,
Geiselhardt, Fatouros, unpublished data). Leaves of A. thaliana release only low amounts of terpenoids, whereas the majority of
the terpenoids of this plant species is emitted from the owers
(Chen et al., 2003).
However, egg deposition by P. brassicae on leaves of Brussels
sprouts and A. thaliana induces changes of the leaf surface that arrest a host searching egg parasitoid at this leaf, and thus, intensies
host search in the vicinity of eggs (Fatouros et al., 2005; Hilker,
Blenn, Geiselhardt, Fatouros, unpublished data). In Brussels
sprouts, oviposition-induced leaf surface changes are detectable
only 3 days after egg deposition. Leaves with freshly laid eggs
(12 days old) also elicit a positive response in the egg parasitoid
upon contact; however, this positive response is not due to oviposition-induced leaf changes, but to kairomonal effects of residues
left by the buttery during egg deposition (e.g. scales). Again, as
has been discussed for the oviposition-induced release of leaf volatiles, also oviposition-induced leaf surface changes seem to be
limited to a certain, ecologically relevant time window; this strategy might limit the costs for the oviposition-induced, indirect defence. The leaf surface changes in Brussels sprouts are restricted
to the leaf carrying an egg mass of P. brassicae; no systemic effects
are detectable (Fatouros et al., 2005). Chemical analyses of the oviposition-induced leaf surface changes in A. thaliana revealed that
induced leaves differ from egg-free controls by the quantitative
composition of leaf surface compounds; no qualitative differences
have been found so far (Hilker, Blenn, Geiselhardt, Fatouros,
unpublished data).
In addition to the above-mentioned effects of egg deposition on
the plants surface that serve indirect plant defence involving egg
parasitoids, eggs can also induce changes of plant tissue (including
the surface) serving direct defence against the eggs or the hatching
larvae. Egg deposition by several insects has been shown to induce
formation of necrotic tissue directly at the site where eggs are attached to the leaf. This necrosis is associated with dehydration and
desiccation of the surface. Eggs do not stick well on a dry leaf surface and easily fall off the plant. Eggs that drop down suffer much
higher risks of mortality than eggs on the plant. In humid soil, the
risk of infection by pathogens may be much higher. Furthermore,
when herbivorous larvae hatch in the soil instead of starting their
life on a leaf they hardly nd their way back to the host plant (Balbyshev and Lorenzen, 1997). Formation of necrotic leaf tissue in response to eggs has been shown in several plantherbivore
interactions. Eggs of the butteries P. brassicae and Pieris rapae L.
can induce necrotic zones on leaves of mustard plants, Brassica nigra L. (Shapiro and DeVay, 1987). Leaves of A. thaliana show no visible formation of necrotic tissue at the sites of egg deposition by P.
brassicae, but they accumulate callose and produce H2O2 at these
sites (Little et al., 2007). Such hypersensitive response (HR) or
HR-like response to eggs was also found in a clone of a hybrid of
Solanum L. spp.; plants of this clone form necrotic tissue around
egg masses of the Colorado potato leaf beetle, Leptinotarsa decemlineata Say (Balbyshev and Lorenzen, 1997).
Instead of formation of necrotic tissue and HR-like responses,
some lines of pea (Pisum sativum L.) form neoplasms on the surface
of their pods in response to egg deposition by the pea weevil, Bruchus pisorum (L.), and the cowpea weevil, Callosobruchus maculatus
(F.) (Doss et al., 2000). These bruchid beetles lay eggs on the surface of a pea pod, the hatching larvae chew holes into the pod
and develop inside the pod. The neoplasm that is formed where an
egg is laid elevates the egg from the pod surface. The exposed egg
does not stick so tightly anymore to the surface and easily drops
down. Again, like described above for eggs detached from necrotic
leaf tissue, eggs that drop down from a pea pod suffer a high risk of
mortality. If an egg does not fall off a pea pod with a neoplasm, the
hatching larva needs to penetrate the tissue protuberance or needs
to circumvent it to get inside of the pea pod. These challenges
increase the risk of larval mortality (Doss et al., 2000).
3.2.3. Egg deposition affects biosynthesis of non-volatile plant internal
secondary metabolites
While effects of eggs on the plants volatile emission and on the
changes of plant tissue detectable at the surface have been addressed in several studies, little knowledge is available on possible
effects of eggs on secondary plant metabolites biosynthesized and
kept inside a cell. How could a plant benet when responding to
eggs by a change of its internal secondary metabolites, while the
egg is touching just the surface? If the egg would induce a sustainable change of the plants secondary metabolism in such a way that
the hatching larvae would face metabolites that impair larval
development, the egg deposition would prepare direct plant defence against larval feeding.
In order to investigate whether egg-induced defences inuence
plant defence against feeding larvae, we compared performance of
two types of pine sawy larvae (D. pini): (1) larvae that started
their life on the pine twig (P. sylvestris) where they hatched from
eggs and (2) larvae that started larval development on an egg-free
pine. Two weeks after larval hatching, both types of larvae were
transferred to egg-free pine twigs since in nature, hatching larvae
also move to egg-free pine twigs after having fed up the needles
of the twig where they hatched from eggs. The results showed that
young larvae starting to feed on a previously egg-laden twig gain
signicantly less weight than larvae starting their life on egg-free
tissue. These negative effects on neonate larvae that fed on needles
with prior eggs carry over to the entire juvenile development
(about 4 weeks long): mortality rates of these larvae are higher
and their duration of development is signicantly longer than in
larvae that initially fed on egg-free pine. The egg-induced effects
on the performance of the sawies are even detectable in the next
generation. Females that developed from larvae starting their life
on previously egg-laden pine show reduced fecundity compared
to females that spend their entire juvenile development on eggfree pine. These performance studies clearly show that egg deposition can warn the plant of future feeding damage (Beyaert, I.,
Koepke, D., Stiller, J., Hammerbacher, A., Schmidt, A., Gershenzon,
J., Hilker, M., unpublished data).
Future studies need to elucidate the phytochemical differences
between pine foliage induced by both sawy egg deposition and
feeding larvae on the one hand and egg-free pine foliage induced
by larval feeding only on the other hand. Such studies will also
show whether insect egg deposition can prime a plants defensive
phytochemial response to feeding larvae. Priming of anti-herbivore
defence in an undamaged plant is well known to be triggered by
volatiles released from herbivore-infested plants that are in the
vicinity of the yet undamaged plant. The undamaged plant may assess the risk of herbivore damage by listening to the damage of
the infested plant (Choh and Takabayashi, 2006; Engelberth
et al., 2004; Frost et al., 2008; Heil and Kost, 2006; Heil and Ton,
2008; Par et al., 2005). The study of pine and pine sawies described above suggests that a plant noticing and responding to
insect eggs can get ready for battle against feeding herbivores
(Conrath et al., 2006; Frost et al., 2008).
In contrast, a study by Bruessow et al. (2010) found that weight
of 8-day-old P. brassicae larvae feeding on A. thaliana leaves treated
with extract of crushed eggs did not differ from those feeding on
1619
untreated leaves, whereas weight of 8-day-old larvae of the generalist moth Spodoptera littoralis Boiduval was even higher on extract-treated leaves compared to untreated controls. Future
studies need to elucidate whether egg-mediated plant effects on
herbivore performance vary with the plantinsect system studied
and whether treatment of leaves with extracts of crushed eggs
has the same effect on larval performance as egg deposition.
Egg-induced changes of the non-volatile secondary plant
metabolites may also have directly detrimental effects on the eggs
if the harming metabolites exude and reach the eggs. This is the
case in rice plants which produce benzyl benzoate in response to
egg deposition by the planthopper Sogatella furcifera (Horvath).
When the plant tissue responds to egg deposition by formation
of a watery lesion, benzyl benzoate comes in contact with the eggs
and has ovicidal activity. More than 80% of the eggs die within two
days when the plant forms a watery lesion, whereas more than 80%
survive and show regular embryo development when the plant
does not respond by a watery lesions to the egg deposition. Benzyl
benzoate was detected in the extract of watery oviposition lesions
(Seino et al., 1996; Suzuki et al., 1996).
Egg-induced changes of iridoid glycosides (IG) of Plantago
lanceolata L. have been discussed by Reudler Talsma et al. (2008).
Leaves with eggs of the buttery Melitaea cinxia L. were found to
contain higher IG concentrations than egg-free leaves. However,
the results of this study suggest that the buttery prefers leaves
with high IG concentration for oviposition rather than an inductive
effect of eggs on IG biosynthesis.
4. Interacting factors of plants and insect eggs

4.1. Egg-associated secretions elicit plant responses
A recent review summarised and discussed current knowledge
on elicitors of plant direct and indirect defence against insect eggs
(Hilker and Meiners, 2010). In short, these elicitors are either released by the egg-laying female or have been detected in secretions
associated with the eggs and adhering them to plant. Direct plant
defence against eggs by formation of neoplasms is elicited by
mono- and bis-(3-hydroxypropanoate)esters of monounsaturated
C22-diols or mono- and diunsaturated C24-diols. These lipid-derived elicitors are called bruchins since they were isolated from
bruchid beetles inducing formation of neoplasms on pea pods
(see Section 3.2.2) (Doss et al., 2000). An elicitor of indirect plant
defence against eggs by change of surface chemistry arresting
egg parasitoids is benzyl cyanide, a compound present in the sticky
secretion associated with eggs of P. brassicae. The P. brassicae females receive these compounds from males during mating; the
males transfer the compound as anti-aphrodisiac to ensure their
paternity (Andersson et al., 2000; Fatouros et al., 2008a,b). In contrast to these low molecular elicitors, the elicitor of indirect defence against eggs in the diprionid sawy D. pini and the elm leaf
beetle X. luteola is a proteinaceous compound released with oviduct secretion enclosing the eggs. This secretion looses elicitor
activity when treated with a proteinase (Hilker et al., 2005; Meiners, unpublished data). Thus, even though only few elicitors of
plant defence against eggs have been studied so far, their chemistry varies broadly.
The plant tissue directly exposed to the elicitors of plant defence against eggs ranges from the plant cuticle over mesophyll
cells to parenchymatic leaf tissue. The elicitor benzyl cyanide associated with egg secretion of the buttery P. brassicae needs to penetrate the plant cuticle since eggs are laid on the leaf surface
without any visible leaf wounding; the proteinaceous elicitor
associated with eggs of the elm leaf beetle comes into contact with
the mesophyll cells of the leaves since the egg-laying female
1620
removes the epidermis; the proteinaceous elicitor present in the

secretion enclosing sawy eggs is deeply inserted into a pine needle and faces parenchymatic tissue in the ovipositional wounding
of the needle. So far, the mode of action of the elicitors of oviposition-induced plant defence is unknown, and future studies need to
address the question whether they e.g. bind to a receptor or are
forming channels in cell membranes (compare Alborn et al.,
1997; Engelberth et al., 2000, for elicitors of plant defence against
feeding insects).
Ovipositional wounding per se (without eggs or egg secretion)
has so far not been shown as elicitor of induced plant defence
against eggs. However, even very tiny wounds like the rupture of
foliar glandular trichomes in tomato plants (Solanum tuberosum
L.) by an insect touching the leaf have been found to induce defence genes (e.g. proteinase inhibitor 2, or PIN2, a gene encoding
a JA-regulated proteinase inhibitor) for several hours (Peiffer
et al., 2009). An insect laying eggs may also destroy these glandular
trichomes. It is yet unknown whether such effects induced by trichome rupture during oviposition may inuence plant defensive
responses against eggs.
4.2. Phytohormones and plant defence genes respond to eggs
Phytohormones are involved in conveying the information
about egg deposition within the plant from the site of egg deposition to other parts. Treatment of elm and pine with JA leads to release of volatiles that are attractive to egg parasitoids (Hilker et al.,
2002a; Meiners and Hilker, 2000). In pine, both egg deposition
and treatment with JA induce an increase of emission of (E)-bfarnesene, a key component for attraction of egg parasitoids
attacking pine sawy eggs (Mumm et al., 2003). However, while
egg deposition by a sawy on pine leads to a reduction of ethylene
emission compared to egg-free controls, treatment of pine with JA
results in an increase of ethylene emission (Schroeder et al., 2007).
These ndings indicate that other phytohormones than JA are additionally involved in activation of pine defence against sawy eggs.
Bruessow et al. (2010) showed that salicylic acid accumulates at
the site where eggs of P. brassicae are laying on a leaf of A. thaliana;
they suggest that a cross-talk between jasmonic acid and salicylic
acid mediates plant responses to insect eggs. Thus, phytohormones
acting in concert with jasmonic acid are probably important for
signalling the presence of eggs to a plant.
Transcriptional changes in response to insect egg deposition
have been shown in several plantegg interactions:
P. sativum bruchid eggs. The change of plant surface tissue and
formation of neoplasms on pea pods after egg deposition by bruchid beetles is associated with the up-regulation of several defence-relevant genes encoding enzymes involved in isoavone
phytoalexin biosynthesis, in the octadecanoid pathway and nodule
formation (Cooper et al., 2005; Doss et al., 2000; Doss, 2005).
Brassica L. and Arabidopsis Heynh. Pieris Schrank eggs. Egg
deposition by P. brassicae on leaves of Brussels sprouts induces
transcriptional changes of genes that may lead to the surface
changes arresting egg parasitoids. For example, a-expansin EXPA15
and xyloglucan endotransglucosylase/hydrolase XTH6, genes involved in cell wall metabolism, are induced by egg deposition. In
addition, transcription of a wide range of other genes involved in
several metabolic processes was found to change in response to
egg deposition. Since the oviposition-induced changes of leaf surface chemistry in Brussels sprouts were detected in the vicinity
of P. brassicae egg masses, transcript levels of leaf tissue next to
the eggs were determined (Fatouros et al., 2008a,b). Little et al.
(2007) took the leaf tissue directly underneath the eggs to determine the transcriptional response of leaves of A. thaliana to 3day-old P. brassicae eggs. They showed signicant transcriptional
changes of hundreds of genes involved in a wide range of meta-
bolic processes (e.g. photosynthesis, proteolysis, biosynthesis pathways of several plant secondary metabolites, hormone
biosynthesis, fatty acid metabolism, wax biosynthesis). For three
genes encoding pathogenesis related protein PR1, trypsin inhibitor
and chitinase, expression was also measured in the vicinity of eggs
and in egg-free distal leaves of an egg-laden plant. Only PR1 shows
a high expression level in the vicinity of the eggs similar to the one
at the site of eggs, whereas the two other genes show high expression levels only directly at the site where the eggs are laid, but
much lower levels in the vicinity of the site of egg deposition. Future studies need to address the question whether the transcriptional changes of tissue directly underneath the eggs is due to
egg-specic factors or to the fact that tissue underneath the eggs
has no access to light and has glued stomata due to the sticky
egg secretion.
P. sylvestrisD. pini eggs. Scots pine (P. sylvestris) responds to
eggs laid by the pine sawy D. pini on its needles by enhancing
the transcription of two sesquiterpene synthase genes, an (E)-bcaryophyllene/a-humulene synthase (PsTPS1) and a 1(10),5germacradiene-4-ol synthase (PsTPS2) (Koepke et al., 2008). Both
PsTPS1 and PsTPS2 transcripts are signicantly enhanced only in
P. sylvestris, but not in Pinus nigra Arnold laden with eggs of D. pini.
Interestingly, P. sylvestris laden with sawy eggs releases volatiles
attractive to egg parasitoids, whereas P. nigra laden with these eggs
does not. Since enhanced transcription of these genes was also
found only at those time periods when odour was attractive to parasitoids, i.e. 3 days after oviposition, PsTPS1 and PsTPS2 are good
markers for the attractiveness of P. sylvestris to egg parasitoids
(Koepke et al., 2010).
5. Conclusions
The close relationship between plants and insect eggs is not
unidirectional limited to the well known effects of plants on insect
egg deposition and eggs. Evidence is growing that egg deposition
by many herbivorous insects induces changes of plant chemistry
which serve defence of the plant against insect attack at this early
stage prior to larval feeding damage (Hilker and Meiners, 2006).
Future studies on the following key questions will broaden and
deepen our knowledge on interactions between plants and insect
eggs:
1. How species specic are effects and mechanisms of interactions
between plants and eggs? Which common traits are detectable?
So far, the effects of eggs on a plant were found to be very specic to the interacting species (e.g. Koepke et al., 2010; Meiners
et al., 2000; Mumm et al., 2005). Induction of sesquiterpenes
plays a role in several plantegg interactions where plants are
dicotyledonous, whereas eggs laid on a monocotyledonous
grass species did not affect the terpenoid emission, but reduced
emission of a green leaf volatile compound (see Section 3.2.1).
However, further systems need to be studied when trying to
detect common patterns. The high species specicity found so
far requires specicity of the elicitor (the eggs with their secretions touching the plant tissue) and of the responding mechanisms of the plant.
2. What happens between detection of eggs by a plant and change
of transcription of plant defence genes? We know in some
plantinsect egg systems the elicitor of egg-induced defence
and the genes affected with respect to transcription, yet we cannot answer this question. Neither on the cellular nor on a systemic level we know how the signal an egg has been laid is
conveyed inside the plant. The role of phytohormones in plant
responses to insect eggs is puzzling. A few studies indicate that
JA is involved (Hilker et al., 2002a; Meiners and Hilker, 2000),
others suggest a signicant role of SA (Bruessow et al., 2010). A

cross interaction between JA- and SA-mediated processes elicited by oviposition may generate a specic internal plant signal.
The interplay of the hormones might depend on whether egg
deposition is associated with plant damage or not. Future studies need to further address the plant signalling cascades
induced by eggs.
3. What are the costs and benets of a plant responding to insect
eggs? Plants can get rid of insect eggs by detaching them (by
hypersensitive response, formation of neoplasms), by poisoning
them (by an egg-induced plant ovicidal compound) or by killing
them with the help of attracted parasitoids. They may gain benet from these defensive responses to eggs, as they reduce the
number of larvae that would damage the plant if they would
hatch from the eggs (see Section 3.2). However, knowledge on
the costs of these egg-induced plant defences is lacking. So
far, only very few studies investigated egg-induced effects on
photosynthetic activity which is considered one currency
among several others to measure costs of plant defence (Cipollini et al., 2003). Hence, we do not know yet whether plants
responding to insect eggs pay later on by reduced growth,
reproduction or defence against other organisms.
4. Do egg-induced plant responses affect later defence against larvae that hatched from surviving eggs? A plant might take eggs
on its leaves as warning of future larval herbivory and improve
its defence against larvae (Section 3.2.3). In turn, feeding by
adults prior to oviposition might alert the plant to future egg
deposition, and the plant may enhance defences against insect
eggs.
Intensifying our research on these questions will further elucidate the mechanisms and ecological effects of egg-induced plant
responses.
Acknowledgements
We thank Urte Kohlhoff, Freie Universitt Berlin, for correcting
our typing errors and reference list. We are grateful for the support
by the German Research Foundation (Deutsche Forschungsgemeinschaft, DFG ME 1810/4-2, DFG Hi 416/17-1,2 and 416/22).
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Woods, H.A., 2010. Water loss and gas exchange by eggs of Manduca sexta: trading
off costs and benets. J. Insect Physiol. 56, 480487.

Zangerl, A.R., Hamilton, J.G., Miller, T.J., Crofts, A.R., Oxborough, K., Berenbaum, M.R.,
de Lucia, E.H., 2002. Impact of folivory on photosynthesis is greater than the
sum of its holes. Proc. Natl. Acad. Sci. USA 99, 10881091.
Monika Hilker studied biology and chemistry at the

University of Goettingen, Germany. After her diploma
thesis on bark beetle chemical ecology, she started her
Ph.D. studies on infochemicals inuencing insect egg
deposition. She nished her Ph.D. studies in 1986 (Dr.
rer. nat.) and took a position as Assistant Professor at
the University of Bayreuth in Bavaria; here she focused
on chemical ecology of the juvenile stages of leaf beetles
(Chrysomelidae). In 1993, she earned her habilitation in
Zoology (Dr. habil.). Since 1994, she is Full Professor and
head of the Department of Applied Zoology/Animal
Ecology at the Freie Universitaet Berlin. Her major
interest is in the eld of chemoecology of plantinsect interactions, and she puts
special emphasis on eggs of herbivorous insects and factors affecting insect egg
deposition. Currently, she is President of the International Society of Chemical
Ecology and serves as Associate Editor of the Journal of Chemical Ecology.
1623
Torsten Meiners studied biology at the University of

Wuerzburg, Germany, and nished his diploma thesis
on malachiid beetle behavioural ecology in 1994. He
started his Ph.D. studies on infochemicals in plant
herbivoreparasitoid interactions at the Freie Universitaet Berlin in 1995 and nished them with a Dr. rer. nat.
in the beginning of 1999. From 1999 to end of 2000, he
worked rst as post-doc on the ecology of ticks at the
Humboldt Universitaet Berlin. Later, he went for a postdoc to the USA where he studied odour learning
capacities of parasitoids at the University of Georgia.
Furthermore, he stayed for six months at the Chemical
Ecology lab of the Swedish University of Agricultural Sciences in Alnarp where he
worked on insect electrophysiology and behaviour. In the end of 2000, he returned
to Berlin and took a position as Assistant Professor at the Freie Universitaet Berlin;
here he works at the Department of Applied Zoology/Animal Ecology on the
Chemical Ecology of multitrophic interactions. His special research interests are the
roles of chemical and structural diversity of the vegetation and of induced plant
defences on host and host plant location strategies of herbivores and their parasitoids. He is member of the International Society of Chemical Ecology and Associate Editor of BioControl.

Phytochemistry: Monika Hilker, Torsten Meiners

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Phytochemistry 72 (2011) 16121623

Contents lists available at ScienceDirect

Plants and insect eggs: How do they affect each other?

Plants serve as oviposition sites for most herbivorous insects

M. Hilker, T. Meiners / Phytochemistry 72 (2011) 16121623

(LeConte) or the Viburnum L. leaf beetle Pyrrhalta luteola (Mller)

2. Plant effects on insect eggs

M. Hilker, T. Meiners / Phytochemistry 72 (2011) 16121623

2004). Besides lepidopteran species, other well known examples of

M. Hilker, T. Meiners / Phytochemistry 72 (2011) 16121623

Humidity, concentrations of oxygen and carbon dioxide as well as

contribute to the endowment of eggs with plant toxins; males

M. Hilker, T. Meiners / Phytochemistry 72 (2011) 16121623

Scots pine, Pinus sylvestris

Pine sawy, Diprion pini

Schroeder et al. (2005)

Elm leaf beetle, Xanthogaleruca

Meiners (unpublished data)

Elm leaf beetle, Xanthogaleruca

Meiners and Hilker (2000), Wegener et al. (2001)

Spotted stemborer moth, Chilo

Bruce et al. (2010)

Cabbage buttery, Pieris brassicae

Fatouros et al. (2005)

Colorado potato leaf beetle,

Balbyshev and Lorenzen (1997)

On plant secondary metabolism

Scots pine, Pinus sylvestris

Savoy cabbage, Brassica

Mustard, Brassica nigra

Accumulation of callose; production

Thale cress, Arabidopsis

(d) Induction of non-volatile plant secondary metabolites

Little et al. (2007)

Colazza et al. (2004a,b)

Shapiro and DeVay (1987)

Bruchid beetles, Bruchus pisorum;

Doss et al. (2000)

Seino et al., 1996; Suzuki et al., 1996

lower photosynthetic activity than plants which are egg-free, but

2002). The effect of feeding damage on photosynthetic activity

M. Hilker, T. Meiners / Phytochemistry 72 (2011) 16121623

3.2. Insect egg deposition changes the plants secondary metabolism

attractiveness to the parasitoid (Bchel, Malskies, Mayer, Fenning,

M. Hilker, T. Meiners / Phytochemistry 72 (2011) 16121623

The oviposition-induced effects on bean and cabbage show

3.2.2. Egg deposition affects plant surface chemistry

M. Hilker, T. Meiners / Phytochemistry 72 (2011) 16121623

4. Interacting factors of plants and insect eggs

M. Hilker, T. Meiners / Phytochemistry 72 (2011) 16121623

removes the epidermis; the proteinaceous elicitor present in the

M. Hilker, T. Meiners / Phytochemistry 72 (2011) 16121623

others suggest a signicant role of SA (Bruessow et al., 2010). A

Choh, Y., Takabayashi, J., 2006. Herbivore-induced extraoral nectar production in

M. Hilker, T. Meiners / Phytochemistry 72 (2011) 16121623

M. Hilker, T. Meiners / Phytochemistry 72 (2011) 16121623

Monika Hilker studied biology and chemistry at the

Torsten Meiners studied biology at the University of

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