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First published online August 30, 2006
Journal of Experimental Biology 209, 3629-3635 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02416
Effect of host kairomones and oviposition experience on the arrestment behavior of an egg parasitoid
1 Dipartimento di Scienze Entomologiche, Fitopatologiche, Microbiologiche
Agrarie e Zootecniche - Sezione di Entomologia, Acarologia e Zoologia,
Università di Palermo, Viale delle Scienze, Palermo 90128,
Italy
2 INRA, 400 Route des Chappes, BP167, 06903 Sophia Antipolis Cedex,
France
* Author for correspondence (e-mail: colazza{at}unipa.it)
Accepted 28 June 2006
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Key words: Trissolcus basalis, Nezara viridula, host location, infochemical detour, learning
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; Vinson,
1991; Vinson,
1998). An extensive literature exists regarding the origin of
these chemical cues, their general or specific incidence, and the innate or
learned ability of female parasitoids to perceive them
[(Vet and Dicke, 1992;
Godfray, 1994;
Vet et al., 1995;
Quicke, 1997) and references
therein]. According to the `variable response model' developed by Vet et al.
(Vet et al., 1995;
Vet et al., 2003), wasps have
innate responses to each subset of chemical cues used for locating their
hosts, and such responses can be ranked according to their potential effects,
so that the variability of wasp responses to each stimulus should be related
to their potential benefits (Vet and
Groenewold, 1990; Vet et al.,
1990). Through association of innate stimuli with host-derived
stimuli such as successful oviposition, female wasps can enhance their
searching efficacy. Subsequently, the maintenance of such associative
experience is mainly related to whether or not host eggs are successfully
located (Vet et al., 1995;
Vinson, 1998;
Takasu and Lewis, 2003). Any
chemical cue released by a host can act as a kairomone. However, when hosts
are concealed or less active, their presence also can be revealed by chemicals
that are not directly associated with them
(Vet and Dicke, 1992;
Meiners et al., 1997;
Meiners and Hilker, 1997;
Colazza et al., 2004a;
Colazza et al., 2004b). For
example, adult scales lost by Heliothis zea (Boddie) and Sesamia
nonagrioides (Lefebvre) moths induce females of the egg parasitoids
Trichogramma pretiosum Riley and Telenomus busseolae Gahan,
respectively, to search longer on host patches where such cues are present
(Beevers et al., 1981;
Gardner and van Lenteren,
1986; Colazza and Rosi,
2001). In this work we investigated the effects of residues of
adult hosts and oviposition experience on the host location of Trissolcus
basalis (Hymenoptera: Scelionidae), an egg parasitoid of several
pentatomid bugs, including the southern green stink bug, Nezara
viridula (Heteroptera: Pentatomidae), a pest of a wide variety of
economically important crops (Todd,
1989; Colazza and Bin,
1995). Previous studies showed that chemical residues left on the
substrate by both nymphs and adults of N. viridula play a role as
indirect host-derived cues inducing arrestment responses in the parasitoid
females (Colazza et al., 1999).
We developed laboratory experiments to quantify how the hierarchical value of
residues from host adults and oviposition experience can influence the
arrestment behavior of T. basalis females.
The arrestment response of wasps to traces of host adults is a host
location strategy commonly observed in scelionid (Hymenoptera: Scelionidae)
egg parasitoids of pentatomid bugs (Heteroptera: Pentatomidae). To date, the
presence of arresting kairomones has been observed in the following host-egg
parasitoid associations: Nezara viridula (L.) - Trissolcus
basalis (Wollaston) (Colazza et al.,
1999; Salerno et al.,
2006), Murgantia histrionica Hahn - Trissolcus
brochymenae (Ashmead) (Conti et al.,
2003), Eurydema ventrale Klt. - Trissolcus
simoni (Mayr) (Conti et al.,
2004) and Euschistus heros (F.) - Telenomus
podisi (Ashmead) (Borges et al.,
2003). Female wasps that fail to locate host egg masses while
exploring a contaminated area should be less likely to respond to the same
stimulus in the near future, whereas female wasps that successfully located
host egg masses should have their responses reinforced. The objectives of the
present study were thus to determine how wasps' arrestment responses were
influenced by (1) chemical residues left by N. viridula adults, (2)
successful oviposition experience, and (3) repeated encounters with areas
contaminated by host chemical residues.
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Adults of T. basalis emerged from parasitized egg masses were kept in 16-ml glass tubes and fed with a honey-water solution. Egg masses of N. viridula were collected daily and used to maintain cultures of both N. viridula and T. basalis. Single N. viridula egg masses were exposed to three to four female wasps, and then held in the same environmental conditions until adult emergence. Before being exposed to parasitoid females, egg masses of N. viridula used to maintain T. basalis colonies were removed from the original oviposition substrate and glued on a new strip of paper to avoid wasp contact with any possible chemicals residues from adults. For bioassays, female wasps 2-3-days old and naive with respect to both oviposition experience and contact with cues released by N. viridula were individually isolated in a small vial with a drop of honey-water solution and acclimatized in the bioassay room for about 24 h.
Bioassay procedure
Bioassays were conducted in open arenas consisting of a rectangular sheet
of filter paper (40x20 cm; insect:arena surface ratio of about 1:400).
In the middle of each arena, a circular area (6 cm diameter) was defined and
exposed for 30 min to a single adult of N. viridula, leaving the
surrounding area untreated. This was achieved by constraining the N.
viridula adults under a steel mesh cover (6 cm diameter, 1 cm high, 0.01
cm mesh) to ensure constant contact of the bug legs with the filter paper and,
at the same time, to avoid the atmosphere from becoming saturated by any
possible bug volatiles that might have been retained on the filter paper
surface. Filter papers contaminated by bug's faeces were not used for
bioassays. After removing the bug, one female wasp was gently released in the
middle of the circular area and its arrestment behavior was followed by a
video tracking system (see below) until it flew away from or walked off the
whole arena. The arrestment response behavior of scelionid egg parasitoids to
host-contaminated areas is characterized by an initial prolonged motionless
period with the antennae kept in contact with the surface. Then the wasps,
while drumming the surface with the antennae, start to walk slowly with a walk
characterized by a klinotactic response, i.e. variation in orthokinetic and
klinotaxic locomotion activity, so that the resulting tortuous path keeps the
wasps in the contaminated areas. If no host eggs are found, the response
decreases and the normal walking behavior is gradually resumed
(Colazza et al., 1999). Tested
female wasps that did not show the arrestment behavior, and either flew away
or walked off the arena immediately as a consequence of lack of contact of
their antennae with the treated area, were excluded from the analysis. Adults
of N. viridula used to treat the inner circular area were either
males or females taken from the colony and kept isolated about 3 days before
the bioassays. Experiments were carried out in an isolated room
(2.8x2.4x2.0 m) illuminated by two 18 cm long fluorescent tubes.
All experiments were carried out from 09:00 h to 12:00 h and at
26±1°C. Wasps' walking patterns were scanned with a CCD camera
(Sony M370) equipped with a zoom lens and mounted above the center of the
arena. The video camera was connected to a video monitor (Sony PVM 2130QM) and
a desktop PC equipped with a video frame grabber (Miro Pc-TV - Pinnacle
Systems, Mountain View, CA, USA). A composite video signal from the camera was
fed into computerized video tracking and motion analysis software, developed
for the Linux operating system (Colazza et
al., 1999). A threshold value of 1 mm was adopted during the
acquisition process to avoid detection of artifact slight movements caused by
any noise in the system. The arrestment responses of the female wasps were
quantified over the entire arena (pooling both outside and inside the circular
contaminated area) by means of the following parameters: (1) total arena
residence time (s), (2) average walking speed (mm s-1) and (3)
tortuousity index. This last parameter is a spatial index computed from the
coordinates of the wasps (sample rate=15 points s-1). It was
calculated as 1-mp/tl where mp=maximum projection of the
track in a general straight line of the plane, and tl=total length of
the track. The value can range from 0.0 to 1.0, with higher values
corresponding to more tortuous walking paths
(Colazza et al., 1999).
Experimental protocols
Hierarchical value of host chemical residues
A first experiment was done to evaluate a possible hierarchical value of
areas contaminated by chemical residues left by N. viridula females
or males on the arrestment response of T. basalis females. Naive
wasps were tested on host-contaminated areas. They were then recaptured,
isolated in small vials and tested 1 h later on newly treated arenas according
to the following four cross-combinations: (1) experienced and tested on male
traces (MM; N=31), (2) experienced on male traces and tested on
female traces (MF; N=36), (3) experienced on female traces and tested
on male traces (FM; N=35), or (4) experienced and tested on female
traces (FF; N=34).
Oviposition experience
In a second experiment, we investigated the influence of successful
oviposition experience (rewarding experience) on the wasps' arrestment
responses. This second experiment also aimed to quantify the wasps' ability to
associate an oviposition experience with host chemical residues during a
successive visit to a host-contaminated area. Single naive T. basalis
females were released onto a circular area contaminated with residues of host
males or females and with a host egg-mass (five to six eggs) in the middle.
During this phase, the walking pattern of the wasp was not recorded. Then,
experienced wasps (i.e. those that had located the egg-mass and parasitized at
least one egg) were recaptured and kept isolated in a small vial for 1 h. They
were then tested in open arenas treated with chemical residues from host
females or males as previously described, and their walking pattern was
recorded. These tests were run using two combinations: (1) oviposition on
female traces and tested on female traces (female_kairomone_female, f_ko_f,
N=34) or (2) oviposition on male traces and tested on male traces
(male_kairomone_male, m_ko_m, N=30). For T. basalis females,
successful oviposition is known to increase klinokinesis and decrease
orthokinesis in a manner analogous to contact with host chemical residues
(Bin et al., 1993). Thus, to
separate the effect of oviposition experience and host chemical residues,
experienced female wasps tested on uncontaminated areas were used as controls,
leading to two additional treatments: (3) oviposition on female residues and
tested on uncontaminated arena (female_kairomone_blank, f_ko_b,
N=15), or (4) oviposition on male residues and tested on
uncontaminated arena (male_kairomone_blank, m_ko_b, N=15).
Time intervals between successive encounters with contaminated areas
A third experiment was conducted to examine the arrestment behavior of
female wasps encountering successive host-contaminated areas at different time
intervals without successful oviposition (unrewarding experience). Thus, the
same T. basalis females were exposed to four consecutive open arenas
treated with resides of N. viridula females at intervals of 1, 23 and
72 h. After each exposure, wasps were recaptured and kept isolated in a small
vial until the successive test. It has been demonstrated in several parasitoid
species that extended periods without host contact can affect their
host-searching behavior (for a review, see
Jervis and Ferns, 2004).
Therefore, to disentangle the effect of unrewarded experience and increased
duration without successful oviposition on wasps' arrestment behavior, as a
control we used naive female wasps tested at the same time as experienced
females were re-tested. Each treatment was replicated 24 times.
Statistical analysis
Data were first checked for assumptions of normality with a Shapiro-Wilk
test with P=0.05 considered statistically significant. The assumption
of normality was met for walking speed data, whereas data of arena residence
time and tortuousity index were normalized by logarithmic transformation and
arcsine transformation, respectively. Data from the first experiment were
statistically analyzed using Student's t-tests for paired
comparisons. Data from the second experiment and data from the third
experiment concerning naive females tested at defined periods were analyzed by
one-way ANOVA followed by Tukey's HSD post hoc test for multiple
comparisons between the means. Data for the third experiment regarding
experienced female wasps retested on consecutive open arenas were analyzed by
repeated-measures ANOVA followed by Tukey's HSD post hoc test for
multiple comparisons between the means. Contrast analyses between naive and
experienced female wasps from the third experiment were done using
t-tests. All statistical analyses were done using Statistica 6.0 for
Windows (StatSoft Inc., Tulsa, OK, USA).
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Oviposition experience
The arrestment behavior of T. basalis females when successively
tested in arenas contaminated by host chemical residues was influenced by
previous successful oviposition experience (one-way ANOVA; arena residence
time: F3,90=12.76, P<0.001; mean velocity:
F3,90=9.79, P<0.001; tortuosity index:
F3,90=4.15, P=0.008)
(Fig. 2). Rewarded females
re-encountering host female residues (group f_ko_f) showed longer arena
residence time and increased arrestment responses compared to rewarded females
encountering host male residues (group m_ko_m). The influence of oviposition
experience per se on the wasps' arrestment response could be excluded
because females with successful oviposition experience did not show a strong
arrestment response when re-tested on untreated arenas (group f_ko_b). On the
other hand, arrestment responses of rewarded wasps in the presence of host
male residues remained unchanged when they re-encountered host male residues
(group m_ko_m), and the response was similar to that recorded from control
females (group m_ko_b) (Fig.
2). Therefore, positive oviposition experience elicited
host-seeking behavior by T. basalis females only in the presence of
host female residues, but not in the presence of host male residues.
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). Insect
parasitoids eavesdropping on host chemical residues can receive either
directional information about host location (systematic search), or
information inducing them to intensify their host searching behavior (random
search) (Godfray, 1994).
Systematic search seems more commonly adopted by wasps attacking active hosts
where cues are a reliable indication of their presence, as is the case for
Poecilostictus cothurnatus Gravenhorst, a larval parasitoid of pine
looper moth, Bupalus pinarius L, which is able to find hosts
by following the chemical trails left by the moth larvae
(Klomp, 1981). Random search
is expected to be adopted mainly by parasitoids that respond to contact
chemical cues indirectly associated with the hosts
(Vinson, 1991;
Godfray, 1994). Congruent with
this view, T. basalis females seem to adopt a random search for
locating host eggs as a consequence of an arrestment response induced by
chemical residues left by adults of N. viridula. In this way, once on
infested plants, the possibility of finding host eggs are improved as a
consequence of lowered flight propensity, prolonged stay on the plant, reduced
movement, and increased klinokinesis
(Colazza et al., 1999).
However, the decision of T. basalis females to remain in the plant
canopy to search for hosts could be influenced by the reproductive success
accumulated while foraging on plant surfaces contaminated by host residues.
Foraging insect parasitoids are known to learn which environmental stimuli are
associated with rewarding or aversive outcomes to improve their chance of
future host location and hence their reproductive success
(Lewis and Tumlinson, 1988;
Lewis and Martin, 1990;
Vet and Groenewold, 1990;
Petitt et al., 1992;
Turlings et al., 1993;
Dutton et al., 2000). The
results presented in this paper show that T. basalis has an innate
response to host chemical residues, with a strong preference for female
residues. Oviposition experience enhanced the arrestment responses of the
wasps when they were associated with host female residues, and this appears to
be congruent with the form of experience defined as `
-conditioning'
(sensu Vinson, 1998)
where host or host's products can provide a reward to foraging that increases
the innate response to a stimulus. The magnitude of variability observed for
T. basalis females responding to host female chemical residues as a
consequence of oviposition experience seems fairly constant and predictable in
accordance with the `variable response model' developed by Vet et al.
(Vet et al., 1995).
Trissolcus basalis females that were not rewarded by successful
oviposition within a certain amount of time gradually lost their arrestment
response and progressively moved back to a more general host search behavior.
The adaptive meaning of these results may be that chemical residues of female
N. viridula cannot guarantee the presence of host eggs or provide
directional information. Hence, even when searching in areas contaminated by
`promising host cues', it could be adaptive for females to give up and leave
the area if host eggs are not found after a certain amount of time. Generally,
experience effects on `-conditioned' wasps are not permanent
(McAuslane et al., 1991). Our
results showed that the arrestment response of T. basalis females was
influenced by the time elapsed between two successive unrewarding encounters,
leading to the conclusion that about 72 h is the time needed by wasps to
`forget' negative experiences.
Trissolcus basalis females also respond to residues left by males
and nymphs of N. viridula (Colazza
et al., 1999). Moreover, we found that the innate wasp response to
host male residues was not modified by experience gained during the wasp's
foraging activity. We thus can speculate that host residues might convey to
foraging wasp females not only indirect information about host egg presence,
but also direct information on the presence of their host species. The actual
role of host residues on host specificity of T. basalis was recently
addressed by Salerno et al. (Salerno et
al., 2006), who demonstrated that T. basalis females were
able to discriminate between coevolved and non-coevolved host species which
may be present on the same infested plants. An analogous situation could be
predicted for another egg parasitoid, T. brochymenae, the females of
which showed arrestment responses to residues of third and fifth instars, and
adults of M. histrionica (Conti et
al., 2003).
Our study provides a starting point in the understanding of the importance of chemical residues left by adults of N. viridula on the host location behavior of T. basalis females. Further studies are needed to elucidate the intricate processes involved in the host searching behavior of this parasitoid, and to determine the specific compounds used by T. basalis females in locating their hosts and host habitats.
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Acknowledgments |
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|
References |
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|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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Beevers, M., Lewis, W. J., Gross, H. R., Jr and Noldus, D. A. (1981). Kairomones and their use for management of entomophagous insects: X. Laboratory studies on manipulation of host-finding behavior of Trichogramma pretiosum Riley with a kairomone extracted from Heliothis zea (Boddie) moth scales. J. Chem. Ecol. 7,635 -648.[CrossRef]
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.
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]
Colazza, S. and Bin, F. (1995). Efficiency of Trissolcus basalis (Hymenoptera: Scelionidae) egg parasitoid of Nezara viridula (Heteroptera: Pentatomidae) in Central Italy. Environ. Entomol. 24,1703 -1707.
Colazza, S. and Rosi, M. C. (2001). Difference in the searching behaviour of two strains of the egg parasitoid Telenomus busseolae (Hymenoptera: Scelionidae). Eur. J. Entomol. 98,47 -52.
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., McElfresh, J. S. and Millar, J. G. (2004a). Identification of volatile synomones, induced by Nezara viridula feeding and oviposition on bean spp., that attract the egg parasitoid Trissolcus basalis. J. Chem. Ecol. 30,945 -964.[CrossRef][Medline]
Colazza, S., Fucarino, A., Peri, E., Salerno, G., Conti, E. and
Bin, F. (2004b). Insect oviposition induces volatile emission
in herbaceous plants that attracts egg parasitoid. J. Exp.
Biol. 207,47
-53.
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]
Dutton, A., Mattiacci, L. and Dorn, S. (2000). Learning used as a strategy for host stage location in an endophytic host-parasitoid system. Entomol. Exp. Appl. 94,123 -132.[CrossRef]
Gardner, S. M. and van Lenteren, J. C. (1986). Characterization of the arrestment responses of Trichogramma evanescens.Oecologia 68,265 -270.[CrossRef]
Godfray, H. C. J. (1994). Parasitoids: Behavioral and Evolutionary Ecology. Princeton, NJ: Princeton University Press.
Jervis, M. A. and Ferns, P. N. (2004). The timing of egg maturation in insects: ovigeny index and initial egg load as measures of fitness and of resource allocation. Oikos 107,449 -460.[CrossRef]
Klomp, H. (1981). Parasitic wasps as sleuthhounds. Response of ichneumonid to the trail of its host. Neth. J. Zool. 31,762 -772.
Lewis, W. J. and Martin, J. (1990). Semiochemicals for use with parasitoids: status and future. J. Chem. Ecol. 16,3067 -3089.[CrossRef]
Lewis, W. J. and Tumlinson, J. H. (1988). Host detection by chemically mediated associative learning in a parasitic wasp. Nature 331,257 -259.[CrossRef]
McAuslane, J. H., Vinson, S. B. and Williams, H. J. (1991). Influence of adult experience on host microhabitat location by the generalist parasitoid Campoletis sonorensis (Hymenoptera: Ichneumonidae). J. Insect Behav. 4, 101-103.[CrossRef]
Meiners, T. and Hilker, M. (1997). Host location in Oomyzus gallerucae (Hymenoptera: Eulophidae), an egg parasitoid of the elm leaf beetle Xanthogaleruca luteola (Coleoptera: Chrysomelidae). Oecologia 112, 87-93.
Meiners, T., Koepf, A., Stein, C. and Hilker, M. (1997). Chemical signals mediating interactions between Galeruca tanaceti L. (Coleoptera: Chrysomelidae) and ist egg parasitoid Oomyzus galerucivorus (Hedqvits) (Hymenoptera: Eulophidae). J. Insect Behav. 10,523 -539.
Petitt, F. L., Turlings, T. C. J. and Wolf, S. P. (1992). Adult experience modifies attraction of the leafminer parasitoid Opius dissitus (Hymenoptera: Braconidae) to volatile semiochemicals. J. Insect Behav. 5, 623-634.[CrossRef]
Quicke, D. L. J. (1997). Parasitic Wasps. London: Chapman & Hall.
Salerno, G., Conti, E., Peri, E., Colazza, S. and Bin, F. (2006). Kairomone involvement in the host specificity of the egg parasitoid Trissolcus basalis. Eur. J. Entomol. 103,311 -318.
Takasu, K. and Lewis, W. J. (2003). Learning of host searching cues by the larval parasitoid Microplitis croceipes.Entomol. Exp. Appl. 108,77 -86.[CrossRef]
Todd, J. W. (1989). Ecology and behavior of Nezara viridula. Annu. Rev. Entomol. 34,273 -292.[CrossRef]
Turlings, T. C. J., Wäckers, F. L., Vet, L. E. M., Lewis, W. J. and Tumlinson, J. H. (1993). Learning of host-finding cues by hymenopterous parasitoids. In Insect Learning: Ecological and Evolutionary Perspectives (ed D. R. Papaj and A. C. Lewis), pp. 51-78. New York: Chapman & Hall.
Vet, L. E. M. and Dicke, M. (1992). Ecology of infochemical use by natural enemies in a tritrophic context. Annu. Rev. Entomol. 37,141 -172.
Vet, L. E. M. and Groenewold, A. W. (1990). Semiochemicals and learning in parasitoids. J. Chem. Ecol. 16,3119 -3135.[CrossRef]
Vet, L. E. M., Lewis, W. J., Papaj, D. R. and van Lenteren, J. C. (1990). A variable-response model for parasitoid foraging behavior. J. Insect Behav. 3, 471-490.[CrossRef]
Vet, L. E. M., Lewis, W. J. and Cardé, R. T. (1995). Parasitoid foraging and learning. In Chemical Ecology of Insects. Vol. 2 (ed. R. T. Cardé and W. J. Bell), pp. 65-101. New York: Chapman & Hall.
Vet, L. E. M., Lewis, W. J., Papaj, D. R. and van Lenteren, J. C. (2003). A variable-response model for parasitoid foraging behavior. In Quality Control and Production of Biological Control Agents: Theory and Testing Procedures (ed. J. C. van Lenteren), pp. 25-39. Wallingford: CABI Publishing.
Vinson, S. B. (1984). Parasitoid-host relationships. In Chemical Ecology of Insects (ed. R. T. Cardé and W. J. Bell), pp. 205-233. New York: Chapman & Hall.
Vinson, S. B. (1991). Chemical signals used by parasitoids. Redia 74,15 -42.
Vinson, S. B. (1998). The general host selection behavior of parasitoid Hymenoptera and a comparison of initial strategies utilized by larvaphagous and oophagous species. Biol. Control 11,79 -96.[CrossRef]
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