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First published online May 29, 2009
Journal of Experimental Biology 212, 1825-1831 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.028308
A finely tuned strategy adopted by an egg parasitoid to exploit chemical traces from host adults
1 Dipartimento di Scienze Agrarie e Ambientali, Università di Perugia,
Italy
2 Dipartimento di I.T.A.F., Università di Palermo, Italy
3 Dipartimento di S.En.Fi.Mi.Zo., Section of Acarology, Entomology and Zoology,
Università di Palermo, Italy
* Author for correspondence (e-mail: salerno{at}unipg.it)
Accepted 28 March 2009
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: Trissolcus brochymenae, Murgantia histrionica, egg parasitoid, indirect host-related cues, arrestment response
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Vet and Dicke, 1992).
Additionally, the quality of the host strongly affects parasitoid fitness in
terms of development time, survival to the adult stage, size and fecundity
(Godfray, 1994). Therefore,
for insect parasitoids, hosts represent a limited resource as their
nutritional status can decay rapidly over time. Consequently, parasitoids that
utilize chemical cues to efficiently find and exploit high quality hosts
improve their fitness (van Alphen and Vet,
1986; Godfray,
1994).
The quality of eggs can decrease rapidly with age (as embryo development
proceeds) so egg parasitoids prefer to lay in fresh eggs
(Strand, 1986;
Vinson, 1998). To cope with
such limited time windows of host availability, egg parasitoid females have
evolved specific strategies to exploit direct host-related cues associated
with the presence of suitable host eggs
(Romeis et al., 2005;
Hilker and Meiners, 2006;
Fatouros et al., 2008). For
example, in studies with the egg parasitoid Trissolcus basalis
(Hymenoptera: Scelionidae), it was shown that female wasps most successfully
accept the eggs of their main host, Nezara viridula (Heteroptera:
Pentatomidae), when they are newly laid, up to approximately 72 h old
(Wilson, 1961;
Bin et al., 1993). Follow-up
investigations showed that T. basalis responds to volatile synomones
emitted by bean leaves onto which an egg mass has been oviposited
(Colazza et al., 2004).
However, the production of such oviposition-induced synomones is influenced by
the age of the eggs. In fact, bean leaves bearing eggs that are 72–96 h
old still attract the parasitoid whereas leaves bearing hatched eggs (
120
h old) do not (Colazza et al.,
2004). Similar evidence has been found for the females of
Oomyzus gallerucae (Hymenoptera: Eulophidae), the egg parasitoid of
the elm leaf beetle Xanthogaleruca luteola (Coleoptera:
Chrysomelidae) (Hilker and Meiners,
2006). Plants can also produce contact synomones as a consequence
of herbivore egg deposition and these direct host-related cues are perceived
by parasitoids only when they walk on the damaged plants
(Conti et al., 2006;
Fatouros et al., 2008). In
addition, a wasp's arrestment response to contact synomones is influenced by
the age of the eggs, as has been shown for egg parasitoids attacking some
pests of cabbage plants, e.g. Trichogramma brassicae and
Trichogramma evanescens (Hymenoptera: Trichogrammatidae), parasitoids
of Pieris brassicae (Lepidoptera: Pieridae)
(Fatouros et al., 2005;
Fatouros et al., 2007), and
Trissolcus brochymenae Ashmead (Hymenoptera: Scelionidae), a
parasitoid of Murgantia histrionica Hahn (Heteroptera: Pentatomidae)
(Conti et al., 2006).
These findings indicate that direct host-related chemical cues provide egg
parasitoid females with reliable information on the presence of host eggs of a
suitable age. However, during the host location process, egg parasitoid
females can also `eavesdrop' on chemical cues arising from the activities of
stages of the host other than the eggs. Examples of such indirect host-related
cues are host pheromones and allomones, the kairomones from the scales of
adult Lepidoptera or the kairomones from the traces left behind by adult
pentatomids while moving on the plant (for a review, see
Fatouros et al., 2008). The
ability to exploit indirect host-related cues is broadly adopted by egg
parasitoid females (Vinson,
1998; Fatouros et al.,
2008). These cues mainly enable egg parasitoid females to arrive
in the vicinity of host eggs on the plant. However, as opposed to direct
host-related cues, indirect host-related cues could be less reliable
indicators of the age of egg, as is the case of wasps that exploit the sex
pheromones of herbivores that oviposit far from the mating sites
(Powell, 1999). Other indirect
host-related cues can endow foraging parasitoids with more detailed
information concerning the physiological condition of the hosts, such as
gravid females contaminated by the volatile anti-aphrodisiac pheromone that
becomes more attractive for phoretic egg parasitoids
(Fatouros et al., 2005;
Fatouros et al., 2008).
However, spying on host sexual signals may not be effective for non-phoretic
egg parasitoid females as was demonstrated, for example, for two egg
parasitoids, one phoretic and the other non-phoretic, that attack the same
host Podisus maculiventris (Heteroptera: Pentatomidae)
(Bruni et al., 2000). Females
of the phoretic egg parasitoid Telenomus calvus (Hymenoptera:
Scelionidae) respond to the synthetic pheromone of the host whereas females of
the non-phoretic egg parasitoid Telenomus podisi (Hymenoptera:
Scelionidae) do not (Bruni et al.,
2000).
Among the possible indirect host-related cues, the chemical residues left
on a substrate by host adults while moving around play a relevant role. The
main evidence for this phenomenon comes from studies of pentatomid insects and
their egg parasitoids, such as N. viridula – T. basalis
(Colazza et al., 1999;
Peri et al., 2006), M.
histrionica – T. brochymenae
(Conti et al., 2003;
Conti et al., 2004),
Eurydema ventrale (Heteroptera: Pentatomidae) – Trissolcus
simoni (Hymenoptera: Scelionidae)
(Conti et al., 2004) and
Euschistus heros (Heteroptera: Pentatomidae) – Telenomus
podisi (Borges et al.,
2003). Once in contact with host footprints, egg parasitoids adopt
a motivated searching behavior characterized by a variation in locomotion
activity, which stimulates them to intensively search on patches where
footprints are present (Colazza et al.,
1999; Borges et al.,
2003; Conti et al.,
2003). Such prolonged searching increases the probability of
locating host eggs; this seems especially critical for parasitoids that attack
host species that are polyphagous and normally lay their eggs far from the
mating site (Colazza et al.,
1999; Fatouros et al.,
2008). Under such circumstances, cues associated with host males
would be of minimal use to egg parasitoids because these cues would not help
the parasitoids to locate eggs. Instead, egg parasitoid females should
optimize their sensitivity to cues produced by host females. The available
data supports this scenario, because egg parasitoid females demonstrate the
ability to discriminate between chemical residues left by females and males of
their pentatomid hosts (Colazza et al.,
1999; Conti et al.,
2004).
A prediction of the concept of dietary specialization and infochemical use
in natural enemies is that specialist species' use specific cues more
frequently than generalist species' (Vet
and Dicke, 1992; Steidle and
van Loon, 2003). Therefore, consistent with this concept, egg
parasitoid species with a narrow host range should have developed a strategy
finely tuned to exploit traces left by host females in a physiological
condition that could ensure access to newly laid eggs.
To test this prediction, a series of experiments were developed to
investigate whether the exploitation of host chemical footprints by an egg
parasitoid is influenced by the physiological condition of the host. The
Nearctic association T. brochymenae – M. histrionica
study model was used; this association qualifies as a `specialist at host/prey
and nearly at host plant/feeding substrate level' (sensu
Vet and Dicke, 1992;
Steidle and van Loon, 2003).
In fact T. brochymenae has been recorded from 11 pentatomid species
belonging to the same family (Salerno,
2000), and the harlequin bug M. histrionica attacks only
Brassicaceae and Capparidaceae (McPherson,
1982).
In this paper, first we investigated the ability of the egg parasitoid to discriminate host gender on the basis of the host's varied physiological condition, i.e. virgin adults, mated adults or mated parous females. We will demonstrate that female wasps prefer footprints from mated host females but only when they had not yet laid eggs. Second, we studied the role of host mating, which affects the parasitoid's preferences for the traces left by mated females. We will show that the wasp's preference for mated females is strongly associated with the full transfer of sperm and associated substances to the female during copulation. Third, we used dissected body parts from mated host adults to study the origin of the contact kairomone. We will provide evidence that compounds mediating the arrestment of T. brochymenae females are derived from the host cuticle, and that compounds enabling female wasps to distinguish between mated males and mated females are present on the host legs.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). Every 2–3 days, nymphs of the last instar were
individually isolated by gently transferring them using a fine brush into a
single plastic pot (Ø=40 mm, height=65 mm), and providing them with
water and a portion of cabbage. These nymphs were observed daily until adult
emergence, so that individuals of known ages were continuously available for
the experiments. The colony of T. brochymenae was reared on eggs of
M. histrionica, and adult wasps were kept in 85 ml glass tubes and
fed small drops of Safavi diet (Safavi,
1968). After emergence, male and female parasitoids were kept
together to allow mating. In all of the experiments, female wasps were
2–3 days old, mated and naïve for adult host chemicals. Female
wasps used for experiments were individually isolated in small vials
16–17 h before the bioassays and allowed to acclimatize in the bioassay
room for at least 30 min before bioassays.
Bioassays procedure
All behavioral assays were conducted in open arenas consisting of
rectangular filter paper sheets (340x240 mm). In the center of the open
arena, a 6 cm diameter circle (2827 mm2, representing about 3.5% of
the entire arena surface) was treated with the test stimuli described below,
while the rest of the arena was left untreated. Arenas not contaminated were
used as controls. A single female wasp was gently released onto the center of
the treated area. Wasps that soon after their release displayed typical
arrestment responses, i.e. with the antennae held in contact with the arena
surface, were scored as `response'. Wasps that did not show the arrestment
response were recaptured and retested approximately 1 min later. After three
unsuccessful trials, wasps were considered `non-responsive'. The movements of
the parasitoids over the entire arena were recorded with a video tracking and
motion analysis system (for details, see
Colazza et al., 2007). The time
spent by female wasps in the whole arena until they flew away or walked off
was scored as the arena `residence time' (s). This parameter properly
describes the wasp searching behavior, which is characterized by returning
several times to the treated area followed each time by an examination of the
surface around the treated area. When doing a comparative bioassay, the
different treatments were tested on several days and they were alternated on
the same day after having tested a group of wasps for each arena. All
experiments were carried out from 09:00 h–14:00 h, in an isolated room
at 26±1°C, with the arena illuminated by two 180 mm-long
fluorescent lights (full spectrum 5900 K, 11 W; Lival, Sipoo, Finland).
Parasitoid discrimination of host sex as a function of physiology
In order to examine the wasp's ability to discriminate between host
genders, females of T. brochymenae were exposed to open arenas
contaminated with traces left by adults of M. histrionica in the
following combinations: (1) virgin females vs virgin males; (2) mated
females vs mated males; and (3) mated parous females (one egg mass
laid) vs mated males. Open arenas not contaminated were used as
controls. Virgin adults were obtained from adults that were kept individually
separated from the time of emergence. Mated adults were obtained from pairs
that had copulated and then, immediately after mating, were separated and kept
individually isolated for 24 h before the experiment. Mated parous females
were obtained from mated females that were kept isolated after mating and
checked regularly until they had deposited their first clutch of eggs and were
then used for the experiments approximately 24 h later. Virgin adults and
mated adults were used in the bioassays at the age of approximately
10–14 days post-emergence. The age of mated parous females was variable
as the time span between mating and oviposition is not uniform for this
species (G.S., F.F. and E.C., personal observation). In all cases, parous
females that were older than 15 days were not used in our experiments. The
adults used were kept isolated, as described above, in plastic pots
(Ø=40 mm, height=65 mm) with nylon mesh on the top before being tested
in the bioassays. To contaminate an open arena, a single adult for each gender
and physiological condition was kept in place for 1 h and forced to walk on
the filter paper as described by Conti et al.
(Conti et al., 2003). Both
uncontaminated and contaminated open arenas were used to test five responding
female wasps, and the experiment was repeated four times (20 replications) for
a total of 140 tested wasps.
Parasitoid responses to traces left by host adult females with interrupted copulation
In order to examine the influence of mating on the response of T.
brochymenae to traces of M. histrionica adults, female wasps
were exposed to open arenas contaminated with traces left by mated host
females with interrupted copulation at different time intervals vs
mated host females. Open arenas not contaminated were used as controls. Mated
host females with interrupted copulation were obtained from adult pairs that
were allowed to mate and then gently separated after 0.5, 2, 4 or 8 h. The
time interval of 8 h represents about a third of the mean duration of the
first copulation in our laboratory conditions (G.S., F.F. and E.C., personal
observation). Mated females were obtained from pairs that ended the copula.
All of the host adults used for the bioassays were kept isolated for 36 h
before the experiment in plastic pots (Ø=40 mm, height=65 mm) with
nylon mesh on the top. A single host female was used to contaminate an open
arena as described above, and five wasps were tested for each treated and
untreated arena. The experiment was repeated four times for a total of 120
tested wasps.
Presence of sperm and associated substances in the spermathecal bulb and the dilated portion of the spermathecal duct of host adult females with interrupted copulation
Mated females of M. histrionica with interrupted copulation and
mated females, after having been used for the experiment previously described,
were killed by freezing at –18°C for about 30 min and were dissected
in saline solution under a binocular stereo microscope (Leica DMLB, Milano,
Italy). Then, the spermathecal bulb and the dilated portion of spermathecal
duct (Pendergrast, 1957) were
evaluated for the presence of sperm and associated substances. Moreover, the
width of the dilated portion of spermathecal duct was measured using a
micrometric optic device (Leitz, Wetzlar, Germany 16x) fitted to the
stereo microscope. Four individuals were dissected for each condition for a
total of 20 dissected adults. Digital pictures were obtained using a
high-resolution digital camera (Leica DC 300F).
Parasitoid responses to dissected body parts from mated host adults
Mated adults of M. histrionica, frozen at –18°C for
about 30 min, were dissected into scutellum and legs. The scutellum was
selected as a control body part, because it would not be contaminated with any
compounds from the legs during grooming behaviors. Fine scissors were used to
clip off the legs at the coxa level and cut off the scutellum from the
pronotum. A single open arena was treated by wiping with 18 legs and three
scutella dissected from either three mated females or three mated males of
M. histrionica using fine forceps. In particular the tarsi were
gently rubbed for about 1 s on the filter paper to simulate the insect walking
(30 times per each tarsum). The arenas contaminated by scutella were obtained
by rubbing each scutellum for about 30 s. Arenas not contaminated were used as
controls. Each open arena, treated and untreated, was used to test 15 wasps,
and the experiment was repeated twice (30 replications) for a total of 150
tested wasps.
Parasitoid responses to hexane extracts of dissected body parts from virgin and mated host adults
Virgin and mated adults of M. histrionica, frozen at
–18°C for about 30 min, were dissected into entire legs clipped off
at the coxa level, wings, pronotum and scutellum under a binocular stereo
microscope (Leica DMLB). The inside of the pronotal cuticle was cleaned as
thoroughly as possible to remove traces of adhering tissues. Dissected body
parts from three adults were weighed, then placed together in 15 ml glass
vials and extracted with 10 ml of hexane at 30°C for 2 h. After removal of
the body parts, the resulting extracts were evaporated under a gentle nitrogen
stream and redissolved in 1 ml hexane (Chomasolv®, Sigma Aldrich, St
Louis, MO, USA) and stored at –18°C until assayed. Hexane extracts
were tested at doses of one dissected adult equivalent (DAE) by pipetting 333
µl of extracts onto the treatment area of an open arena. The extract was
applied as drops, resulting in a patch distribution all over the arena. Open
arenas treated with 333 µl of pure hexane were used as controls. The
experiments were repeated three times, and each arena was tested with 15
female wasps (45 replications) for a total of 225 tested wasps.
Statistical analysis
The arena residence times of the wasps were evaluated for their normality
and normalized through logarithmic transformation when required. Student's
t-test for independent samples was used to compare the time spent by
female wasps in contaminated vs control arenas. The same test was
applied to compare the parasitoid residence time on host females vs
host males arenas treated with traces, dissected body parts and hexane
extracts (Zar, 1999). The
residence times of the wasps in the arenas contaminated by females with
interrupted copulation at different time intervals were analyzed by one-way
analysis of variance (ANOVA) (Zar,
1999). Due to a lack of significance, the data from the different
time intervals were pooled and compared with mated females and with controls,
using one-way ANOVA and the unequal N Tukey HSD test for multiple
comparisons between the means. All statistical analyses were performed using
Statistica 6.0 [Statsoft, 2001, Vigonza (PD), Italy].
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RESULTS |
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Presence of sperm and associated substances in the spermathecal bulb and the dilated portion of the spermathecal duct of host adult mated females
The sperm and associated substances were found only in the spermathecal
bulb and in the dilated portion of the spermathecal duct of mated adult host
females but not in females with interrupted copulation. In fact, under the
microscope, the spermathecal bulb of mated host females appeared markedly less
transparent and filled with sperm (Fig.
3). The mean width of the dilated portion of the spermathecal duct
in mated females vs females with interrupted copulation was not
significantly different (1.97±0.23 mm in mated host females and
1.72±0.05 mm in host females with interrupted copula, t=1.72;
d.f.=11; P=0.165). However, under the microscope, the dilated portion
of the duct appeared swollen and whitish only in mated females, as a
consequence of the presence of the associated substance transferred from the
male (Fig. 3).
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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;
Conti et al., 2004). However,
such an ability is expressed only by presence of chemical traces left by mated
females that have not yet laid eggs. In all probability, this finely tuned
strategy allows the parasitoid to find newly laid host eggs, as chemical
traces left by mated host females that have not yet laid eggs are strongly
correlated with the moment of oviposition. We might even suggest that this
strategy could be considered as a form of ambush [sensu Vinson
(Vinson, 1998)], because in
this way T. brochymenae could be in the condition of reaching an area
where host eggs are expected to be laid.
The ability to discriminate the host gender was evidenced in another
Trissolcus species, the egg parasitoid T. basalis
(Colazza et al., 1999;
Peri et al., 2006;
Colazza et al., 2007). However,
when considering the spatial correlation with the moment of the oviposition,
T. basalis females seem to adopt a less tuned host gender
discrimination strategy, as they prefer host female traces rather than male
traces at all physiological conditions, i.e. virgin and mated
(Colazza et al., 1999). Such
dissimilarity in these two egg parasitoids T. basalis and T.
brochymenae may be explained in terms of dietary specialization. In fact,
T. basalis should be included in the group `generalist at the host
and the host plant/feeding substrate levels'
(Vet and Dicke, 1992;
Steidle and van Loon, 2003),
as it was recorded from about 90 species of Pentatomidae and Scutelleridae,
and N. viridula is extremely polyphagous
(Todd, 1989). These two
parasitoid species also show different strategies to use direct and indirect
host-related cues, because T. basalis can exploit volatile
oviposition-induced synomones produced within approximately 72 h from
oviposition and host traces to restrict the searching area
(Colazza et al., 2004), while
T. brochymenae does not use volatile oviposition-induced synomones
but uses volatile compounds from the host and reaches the egg masses at the
right age by exploiting chemical traces from mated host females and/or
oviposition-induced synomones perceived upon contact
(Conti et al., 2003;
Conti et al., 2006). Thus, the
following scenario is suggested: these egg parasitoids use host pheromones as
a good indicator of the presence of a species at long-range, they then exploit
contact indirect host-related cues to discriminate the physiological condition
of the host female at medium/close-range.
The preference of T. brochymenae for mated females is strongly
related to the transfer of sperm and associated substances to the female
during copulation. Evidence of the transfer of sperm and associated nutrients
after prolonged copulation has been shown in other pentatomid species
(Schrader, 1960;
Mitchell and Mau, 1969;
Mau and Mitchell, 1978;
Kasule, 1986;
Koshiyama et al., 1993;
Wang and Millar, 1997;
Ho and Millar, 2001a;
Ho and Millar, 2001b).
Moreover, a role of the male secretions as nutrients for the females has been
documented in other insect orders such as Blattodea
(Mullinus and Keil, 1980),
Orthoptera (Gwynne, 1988),
Lepidoptera (Bogges and Gilbert,
1979) and Coleoptera (Boucher
and Huignard, 1987). Zhan and colleagues hypothesized that M.
histrionica males determine the mating status of potential partners on
the basis of the changes in the cuticular chemistry after copulation (Zhan et
al., 2008). In the same way, these variations in the cuticular chemistry may
explain how T. brochymenae can discriminate the physiological status
of the host female.
The compounds that mediated the arrestment response of T.
brochymenae females seem to be part of the host cuticle. In fact, T.
brochymenae females showed arrestment responses when exposed to arenas
treated by tarsi and scutella dissected from M. histrionica mated
adults. In all probability the cuticular hydrocarbons present in the wax layer
of M. histrionica might be involved, as the kairomonal cues are
hexane soluble. However, the involvement of other components in the
elicitation of wasp response such as mono- and dimethyl-branched alkanes and
polar lipids-branched hydrocarbons cannot be excluded. Similar findings have
been demonstrated in N. viridula as chemicals present on the tarsi
and scutella induced motivated searching responses by females of T.
basalis (Colazza et al.,
2007).
The arena residence time of T. brochymenae was significantly
affected by host gender with a different role played by host body parts. In
fact, wasps stayed longer on the arenas treated with legs dissected from mated
females than on arenas treated with the analogous body parts dissected from
mated males. Therefore, the kairomones that play a role as gender-specific
cues seem to be present in the legs of adult M. histrionica, and they
could be secreted by glands found in the legs of M. histrionica (R.
Romani and N. Isidoro, personal communication). By contrast, in the case of
N. viridula, the kairomones, which induce the arrestment response in
T. basalis, are present in the cuticular lipids distributed all over
the body of the insect, even if leg glands similar to those of M.
histrionica were found in N. viridula
(Colazza et al., 2007). The
mechanism used by T. brochymenae to discriminate between chemical
traces left by mated females that have not yet laid eggs and mated males
remains to be investigated.
In conclusion, our results represent an interesting new piece of information regarding the exploitation of indirect host-related cues by egg parasitoids, as they suggest the existence of a new strategy adopted by an egg parasitoid during the host location process.
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Footnotes |
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References |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Bin, F., Vinson, S. B., Strand, M. R., Colazza, S. and Jones, W. A. (1993). Source of an egg kairomone for Trissolcus basalis, a parasitoid of Nezara viridula. Physiol. Entomol. 18,7 -15.[CrossRef]
Bogges, C. L. and Gilbert, L. E. (1979). Male
contribution to egg production in butterflies: evidence for transfer of
nutrients at mating. Science
206, 83-84.
Borges, M., Colazza, S., Ramirez-Lucas, P., Chauhan, K. R., Kramer, M., Moraes, M. C. B. and Aldrich, J. R. (2003). Kairomonal effect of walking traces from Euschistus heros (Heteroptera: Pentatomidae) on two strains of Telenomus podisi (Hymenoptera: Scelionidade). Physiol. Entomol. 28,349 -355.[CrossRef]
Boucher, L. and Huignard, J. (1987). Transfer of male secretions from the spermatophore to the female insect in Caryedon serratus (OL.): analysis of the possible trophic role of these secretions. J. Insect Physiol. 33,949 -957.[CrossRef]
Bruni, R., Sant'Ana, J., Aldrich, J. R. and Bin, F. (2000). Influence of host pheromone on egg parasitism by scelionid wasps: comparison of phoretic and nonphoretic parasitoids. J. Insect Behav. 13,165 -173.[CrossRef]
Colazza, S., Salerno, G. and Wajnberg, E. (1999). Volatile and contact chemicals released by Nezara viridula (Heteroptera: Pentatomidae) have a kairomonal effect on the egg parasitoid Trissolcus basalis (Hymenoptera: Scelionidae). Biol. Control 16,310 -317.[CrossRef]
Colazza, S., Fucarino, A., Peri, E., Salerno, G., Conti, E. and
Bin, F. (2004). Insect oviposition induces volatiles emission
in herbaceous plant that attracts egg parasitoids. J. Exp.
Biol. 207,47
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Colazza, S., Aquila, G., Peri, E. and Millar, J. G. (2007). The egg parasitoid Trissolcus basalis uses n-nonadecane, a cuticular hydrocarbon from its stink bug host Nezara viridula, to discriminate between female and male hosts. J. Chem. Ecol. 33,1405 -1420.[CrossRef][Medline]
Conti, E., Salerno, G., Bin, F., Williams, H. J. and Vinson, S. B. (2003). Chemical cues from Murgantia histrionica eliciting host location and recognition in the egg parasitoid Trissolcus brochymenae. J. Chem. Ecol. 29,115 -130.[CrossRef][Medline]
Conti, E., Salerno, G., Bin, F. and Vinson, S. B. (2004). The role of host semiochemicals in parasitoid specificity: a case study with Trissolcus brochymenae and Trissolcus simoni on pentatomid bugs. Biol. Control 29,435 -444.[CrossRef]
Conti, E., Salerno, G., De Santis, F., Leombruni, B. and Bin, F. (2006). Difese indirette delle piante: i sinomoni per contatto indotti da ovideposizione. Atti Accademia Nazionale Italiana Entomologia. Rendiconti 54,129 -148.
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