Insect oviposition induces volatile emission in herbaceous plants that attracts egg parasitoids
1 Department of S.En.Fi.Mi.Zo. - Entomology Acarology and Zoology,
University of Palermo, Italy
2 Department of Arboriculture and Plant Protection - Entomology, University
of Perugia, Italy
* Author for correspondence (e-mail: colazza{at}unipa.it)
Accepted 30 September 2003
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Summary |
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Key words: Insecta, Nezara viridula, Heteroptera, Pentatomidae, Trissolcus basalis, Scelionidae, systemic induction, oviposition, insect/plant interaction, chemical ecology
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Introduction |
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In the case of hymenopteran parasitoids, studies of their ability to locate
their hosts using host-induced synomones have focused primarily on parasitoids
whose hosts are defoliators. These insects inflict substantial physical damage
on the plant, which induces qualitative and quantitative changes in the
plant's profile of volatiles (Vinson,
1991; Turlings et al.,
1995
; Geervliet et al.,
1994
; van Alphen and Jervis,
1996
; De Moraes et al.,
1998
,
2001
;
Turlings and Benrey, 1998
;
Guerrieri et al., 1999
). These
volatiles can be plant species specific and/or herbivore species specific
(De Moraes et al., 1998
) and
are generally induced by elicitors in the herbivore saliva or oral secretions.
To date, the main elicitors identified include an enzyme, ß-glucosidase,
isolated from the regurgitant of the large white butterfly caterpillar
Pieris brassicae (L.) (Mattiacci
et al., 1995
), and volicitin, a 17-hydroxylated linolenic acid
conjugated with glutamine, isolated from regurgitant of larvae of the beet
armyworm Spodoptera exigua (Hübner) (Alborn et al.,
1997
,
2000
). Other conjugates of
fatty acids and amino acids that induce the release of volatiles by tobacco
(Nicotiana attenuata Torrey ex Wilson) plants damaged by insect
defoliation have also been detected in the regurgitant of larvae of the
tobacco hornworm Manduca sexta (L.)
(Baldwin et al., 2001
;
Halitschke et al., 2001
).
Furthermore, host-induced synomones have now been demonstrated for those
tritrophic systems in which the herbivores have phloem-feeding or
stylet-sheath-feeding habits (Du et al.,
1998
; Guerrieri et al.,
1999
), although the elicitors have not yet been identified.
Plant synomones can also be induced by factors other than insect feeding
activity. For example, insect egg deposition can induce a change in the
profile of the plant volatiles, and these volatiles have been shown to attract
egg parasitoids (for a review, see Hilker
and Meiners, 2002; Hilker et
al., 2002a
). Plants that are able to attract egg parasitoids soon
after herbivore eggs are laid benefit from increasing the parasitoid's
effectiveness (Vinson, 1985
)
and from beginning to defend themselves against insect pests before any damage
has occurred, i.e. before the larvae have hatched from the eggs
(Hilker et al., 2002a
). To
date, detailed studies on oviposition-induced synomones have been carried out
in two tritrophic systems, showing strong similarities. In both cases, the
herbivores feed on perennial plants, the elicitor(s) is present in the oviduct
secretions, the elicitor(s) must contact the wounded plant tissues, and the
signal(s) is produced both locally and systemically
(Hilker and Meiners, 2002
;
Hilker at al., 2002a
).
Recently, preliminary data suggesting the use of oviposition-induced synomones
have been collected for another tritrophic system consisting of leguminous
annual plants, the southern green stink bug Nezara viridula (L.)
(Hemiptera: Pentatomidae) and its egg parasitoid Trissolcus basalis
(Wollaston) (Hymenoptera: Scelionidae) (S. Colazza, A. Fucarino, E. Peri, G.
Salerno, E. Conti and F. Bin, unpublished;
Hilker and Meiners, 2002
).
Here, we present more complete details of this research.
Trissolcus basalis is a solitary egg parasitoid that attacks eggs
of several phytophagous and predatory pentatomid bugs and it is now
distributed worldwide as a result of extensive deliberate introductions for
use as a biological control agent for N. viridula
(Jones, 1988;
Clarke, 1990
). N.
viridula is a highly polyphagous pest that attacks both perennial and
annual plants. In Italy, it has been mainly recorded as a pest of annual
plants (Colazza and Bin, 1995
).
N. viridula egg mass distribution is determined primarily by the
degree of activity and movement patterns of gravid females
(Todd, 1989
). Data taken from
a wide variety of annual crops indicate that there are primary sites for
feeding and mating and then the gravid females disperse to other host plants
for oviposition, so that egg masses are generally laid quite far from the
adult feeding and mating sites (S.C., personal observation). Therefore, we
predicted that T. basalis females would be unlikely to use cues from
undamaged plants or plant cues induced by N. viridula feeding
activity to locate hosts because host egg masses would not be nearby. Instead,
we predicted that the wasps would be more likely to use cues originating from
the host egg masses themselves or from interactions between the egg mass and
the plant tissues as reliable host location cues.
In the present study, we examined whether volatile plant synomones are induced and released as a result of N. viridula oviposition, whether their activity is dependent on a synergistic effect between damaged plants and egg masses, whether the plants respond systemically to the oviposition, and whether egg mass age has an effect on the oviposition-induced synomones.
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Materials and methods |
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Insect cultures
Adults of Nezara viridula (L.) were reared under laboratory
conditions (24±2°C, 70±5% R.H., 16 h:8 h L:D) in plastic
containers (30 cmx20 cmx15 cm) on a diet of sunflower seeds,
seasonal fresh vegetables and water. N. viridula egg masses were
collected daily and used to maintain cultures of both N. viridula and
Trissolcus basalis (Wollaston). Cultures were augmented regularly
with field-collected bugs. The T. basalis colony was established from
wasps emerging from sentinel N. viridula egg masses placed in both
cultivated and uncultivated fields located around Palermo, Italy. Wasps were
kept in the laboratory at an 18-h photophase, a temperature of
24±2°C and an RH of 70±5% and were regularly exposed to
N. viridula eggs for 24 h in glass vials. Parasitized egg masses were
removed and stored in clean glass vials for development. At emergence, adults
were fed with a honey-water solution. Parasitoid females used in bioassays
were from a laboratory culture that had been in culture for no more than 3-5
generations. Each female was mated, naive, 2-3 days old (at which age they
respond well to odours; S.C., personal observation) and isolated individually
for 24 h before the assay in a small vial with a drop of honey-water
solution.
Y-tube olfactometer and general bioassay procedure
Wasps' responses to volatile chemicals were investigated with a dual choice
Y-tube olfactometer (stem 90 mm; arms 80 mm at 130° angle; internal
section 15 mmx15 mm) sandwiched between two glass sheaths as described
by Colazza et al. (1997). An
air stream (medical air, USP, 79% nitrogen and 21% oxygen by volume) was
humidified by bubbling through a water jar and was then drawn through each arm
of the olfactometer (30 ml min-1 per arm). Before entering the
olfactometer arms, each air stream passed through a 600 ml glass jar
containing odour sources described below. The odour sources were randomly
assigned at the beginning of the bioassays and were reversed after testing
approximately five parasitoid females. The responses of 16-38 parasitoid
females were tested for the various treatments and combinations. Tests were
conducted from
09:00 h to 16:00 h. After each trial, the whole system was
rinsed with acetone and baked overnight at 200°C. Female wasps were tested
one at a time, introducing individuals into the olfactometer at the entrance
of the stem and observing the behaviour for 10 min. Behaviours were recorded
on video (monitor Sony® Trinitron; monochrome CCD camera Sony®
SPT-M328CE, zoom lens 12.5-75 mm/F1.8), and a video frame grabber (Studio
PCTV; Pinnacle Systems, Mountain View, CA, USA) was used to digitize the
analogue video signals. Xbug, a video tracking and motion analysis software,
was used to process data (S. Colazza, D. Peri, G. Salerno, E. Peri, M. Lo
Pinto and G. Liotta, unpublished). For each recording, the total time spent in
each olfactometer arm and the linear speed in the whole arena (mm
s-1; sample rate,
6 images s-1) were calculated.
The temperature in the bioassay room was
26°C at all times.
Experiments
The first experiments were designed to investigate female wasps' responses
to undamaged plants versus plants damaged by adult bug feeding and
versus plants damaged by feeding onto which an egg mass had also been
laid. The possible effects of using different plant species on the
oviposition-induced synomones were also tested. Broad bean plants and French
bean plants were singly transferred into a wood-framed, nylon mesh cage (40
cmx40 cmx50 cm) and exposed to 7-10 N. viridula
gravid females for
1-2 days, time enough for the adults to be conditioned
to the new diet and for the females to lay at least one egg mass. About one
hour prior to the bioassays, the bugs were removed and a set of two leaves was
cut from the medium nodes of the treated plants. The cut petioles were wrapped
in wet cotton and inserted in a 1-ml vial filled with distilled water and
sealed with Parafilm®, and the leaves were then transferred to the glass
holding chamber of the bioassay apparatus as described above. Leaves cut from
undamaged plants held in the same conditions were used as controls.
The second experiment was carried out to evaluate whether the wasps'
attraction to oviposition-induced synomones was the result of synergistic
effects between the volatiles from both damaged leaves and the egg mass. The
odour sources consisted of 24-h-old N. viridula egg masses
(60-80 eggs each), laid on nylon screen and collected from rearing boxes
containing 5-8 gravid N. viridula females, and feeding-damaged broad
bean leaves prepared as follows. Volatiles from egg masses alone were tested
versus odours from undamaged broad bean leaves and versus a
treatment consisting of egg masses and feeding-damaged broad bean leaves held
in the same glass jar.
A third experiment was carried out to investigate whether the volatiles
that attract the wasps are released only locally from the damaged leaves
carrying the egg mass or whether the volatiles are produced systemically
throughout the plant. For this purpose, broad bean plants, reared under the
same conditions described for the first experiment, were singly exposed to 3-4
mated N. viridula females in a cage longitudinally divided by a
plastic sheet (40 cmx40 cmx50 cm). Some apical lateral leaves were
carefully pushed through holes in the plastic sheet, and the holes were sealed
at node level with cotton to reduce volatile exchange between the two halves
of the cage. In this way, the test insects were allowed to contact only
4-5 basal lateral leaves of the plant. A few hours after an egg mass had
been laid (less than 24 h), a set of two leaves that had not been in contact
with the bug were cut and prepared as described for the first experiments and
tested versus undamaged broad bean leaves.
A fourth experiment was carried out to study the effect of time since
oviposition of N. viridula egg mass on attraction of the wasps.
N. viridula egg masses became less acceptable to the wasps once they
were 72-96 h old (the eggs become pinkish-yellow due to the embryo development
and hatch at 120 h; Bin et al.,
1993
). Broad bean plants were exposed to 5-7 mated N.
viridula females as described in the first experiment. Once an egg mass
had been laid, the bugs were removed and the plant was held in the environment
chamber until the egg mass was either 72-96 h old or 120 h old and then tested
versus undamaged broad bean leaves.
Statistical analysis
Values for the resident times of parasitoids in each arm of the Y-tube
olfactometer and their linear speeds in the whole arena were normally
distributed (Kolmogorov-Smirnov test) and homoscedastic and were analyzed with
parametric tests (t-test for paired samples; one-way analysis of
variance followed by the Tukey HSD test for multiple comparisons between
means). All the data were analyzed using the Statistica 5.1 Statistical
Package (StatSoft, Inc., Vigonza, Italy).
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Results |
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Volatiles from bug egg masses laid on nylon screen did not attract the parasitoid (t=1.66, P=0.11; Fig. 2A). Furthermore, when combining volatiles from egg masses on nylon screen with those from feeding-damaged leaves that had never carried host eggs, this combination was no more attractive than volatiles from feeding-damaged leaves alone (t=-0.77, P=0.44; Fig. 2B). Therefore, the attractiveness of feeding-damaged leaves carrying egg masses appears to be due to volatiles produced by bug eggs in contact with the leaf and not from a combination of the odours emitted from the egg mass and the leaf held separately.
|
The odours of leaves without egg masses but belonging to a plant with other leaves damaged by feeding and carrying an egg mass emitted volatiles that attracted the parasitoid (t=2.83, P=0.01; Fig. 3). Thus, the attractiveness induced by feeding and oviposition is not confined to the leaves onto which an egg mass has been laid but is systemically induced throughout the plant.
|
The age of the egg mass also influenced the attraction of wasps to leaves bearing egg masses. Thus, feeding-damaged leaves bearing egg mass were attractive to the parasitoid until the eggs were 72-96 h old (t=2.96, P=0.005; Fig. 4A) but not once the eggs had hatched (>120 h; t=-0.77, P=0.44; Fig. 4B).
|
Inside the olfactometer, the wasp's linear speed was significantly affected by the volatiles from different treatments. In the presence of feeding-damaged plant volatiles, wasps walked faster than when in the presence of volatiles from feeding-damaged plants with host egg masses or systemically induced leaves (d.f.=2, F=12.34, P<0.001; one-way ANOVA; Fig. 5).
|
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Discussion |
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Results on our tritrophic system show, for the first time, that annual
plants can produce oviposition-induced synomones. As was suggested by Hilker
et al. (2002a), annual plants,
having a short life cycle and a relatively small biomass, may benefit more
than larger perennial plants from egg parasitoid activity, which indirectly
reduces the number of feeding larvae.
Synomones induced by oviposition by elm leaf beetle and pine sawfly, which
have restricted host ranges, are characterized by a high specificity of
response in their egg parasitoids (Hilker
et al., 2002a). By contrast, N. viridula is highly
polyphagous, developing on more than 150 species within
30 plant
families, although it has a distinct preference for leguminous plants
(Todd, 1989
;
Panizzi et al., 2000
). We
demonstrated that N. viridula oviposition apparently induced
synomones in two different leguminous annual plants. Because of N.
viridula's broad host range, we predict that synomones induced by N.
viridula oviposition will be found in other annual and perennial host
plants.
Unlike elm leaf beetle and pine sawfly, N. viridula females do not
cut or otherwise physically damage the host substrate during oviposition.
Instead, eggs are laid on the leaf surface in clusters that adhere to each
other and to the plant by a sticky oviduct secretion. This secretion
accumulates at the base of the egg while it descends the ovariole, and, once
in contact with the air, the secretion rapidly oxidizes to a light brown film
that extends over the egg mass border (Bin
et al., 1993). Females of elm leaf beetle and pine sawfly also
coat their eggs with oviduct secretion, with two resulting effects. First, the
secretion induces production of synomones in the host plant when in contact
with host tissues wounded during oviposition
(Meiners and Hilker, 1997
;
Hilker et al., 2002b
); elm
leaf beetle females remove leaf lower surface prior to oviposition with their
mouthparts, and pine sawfly females incise pine needles to insert the eggs
(Meiners and Hilker, 2000
;
Hilker et al., 2002b
). Second,
the secretion is used as a contact kairomone that induces host acceptance
behaviour in their egg parasitoids (Bin et
al., 1993
; Meiners and Hilker,
1997
).
To date, our experiments have not yet characterized the elicitor associated
with N. viridula oviposition nor its specific mechanism of action.
Because of the absence of any apparent plant injury at the time of
oviposition, elicitors other than those associated with oviduct secretions may
be possible, such as those associated with the surface chemistry of the eggs,
as is the case with hydrocarbons present in the surface wax of Colorado potato
beetle (Leptinotarsa decemlineata Say) eggs
(Nelson et al., 2003), or even
the presence of egg-associated microorganisms
(Städler, 2002
).
Moreover, in the oviposition-induced synomone cases studied by Hilker et al.,
the influence of adult feeding activity in inducing the synomones has been
excluded (e.g. D. pini adult females do not feed on plants;
Hilker et al., 2002a
). In our
experiments, volatiles released by leaves damaged only by N. viridula
feeding activity were no more attractive than volatiles from undamaged leaves,
but the volatiles produced by the combination of feeding damage and
oviposition appeared to act synergistically. This synergistic activity between
feeding and oviposition seems confirmed by the results of chemical and
behavioural experiments currently in progress on the odours of bean plants
induced by N. viridula adults as a result of their feeding activity,
oviposition activity and feeding and oviposition activity combined (S.
Colazza, J. S. McElfresh and J. G. Millar, personal observation). Synomones
released as a response to attack by phytophagous insects could be produced or
released at the site of the attack, as well as systemically by other parts of
the plant, or the compounds could be produced at the site of the attack,
transported to other sites and released far from the site of the attack
(Dicke, 1999
;
Turlings and Benrey, 1998
).
All the oviposition-induced synomones investigated to date are emitted from
both the leaves carrying the eggs and from insect- and egg-free parts of the
same plant (Hilker et al.,
2002a
; present study). A systemically induced response may benefit
the plant under attack by increasing the amount of synomones produced and
increasing the surface area from which the synomones are released, thus
creating a more apparent signal that could increase parasitoid attraction
(Dicke and van Loon, 2000
and
references therein).
It has been shown that the release of host-induced synomones is timed as a
consequence of several factors such as the cost of defence and/or
synchronization with the wasp's activity
(Turlings and Benrey, 1998).
Host egg resources are ephemeral, because host egg quality rapidly decreases
with time as the host develops (Vinson,
1998
). In our system, the age of host egg mass influences the
acceptance behaviour of T. basalis
(Bin et al., 1993
). Therefore,
it is expected that the production and/or activity of oviposition-induced
synomones should be influenced by the age of the egg mass. Consistent with
this hypothesis, leaves bearing eggs that are 72-96 h old still attract the
parasitoid, while leaves bearing hatched eggs do not.
In conclusion, our knowledge of synomones induced in plants as a result of insect oviposition is still rudimentary, with the specific elicitors, synomones and mechanisms by which they work remaining to be identified. Work currently in progress aims to identify synomones induced by N. viridula oviposition and/or feeding and to examine the time course of their production as first steps in gaining a better understanding of the cues and signals mediating tritrophic interactions in this system.
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Acknowledgments |
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