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1 January 2020 Effects of Volatiles from Clavigralla tomentosicollis Stål. (Hemiptera: Coreidae) Adults on the Host Location Behavior of the Egg Parasitoid Gryon fulviventre (Crawford) (Hymenoptera: Scelionidae)
Apolline Sanou, Fousséni Traoré, Malick Niango Ba, Clémentine L Dabiré-Binso, Barry R Pittendrigh, Antoine Sanon
Author Affiliations +
Abstract

The egg parasitoid Gryon fulviventre is a potential biological control agent of Clavigralla tomentosicollis, a coreid pod-sucking pest of Vigna unguiculata. The host location behavior of naive parasitoid females was studied using a four-armed olfactometer. Two strains of G. fulviventre parasitoids from Burkina Faso and Benin were exposed to odors provided by healthy and infested pods as well as C. tomentosicollis females and males. The time spent in each odor zone was recorded to determine the preference of parasitoid females. Results show that odors from healthy pods, infested pods, and pest females did not attract the parasitoid. However, a significantly attractive response of both strains of G. fulviventre was recorded in the presence of volatiles from males of C. tomentosicollis. Moreover, experiments testing G. fulviventre females’ behavior when simultaneously exposed to volatiles from cowpea pods (healthy and infested) and increasing numbers of C. tomentosicollis males revealed a significantly higher attraction of parasitoid females of both strains by volatiles from ten males of C. tomentosicollis. The results suggest that the males of the insect pest emit a pheromone used as kairomone by parasitoids to locate their host. The conditions determining this attractiveness at field level and its impact on host-searching efficiency are discussed.

Introduction

Insect pests are an important constraint to cowpea (Vigna unguiculata (L.) Walp.) production in the tropics, including in Burkina Faso where the coreid pod-sucking bug, Clavigralla tomentosicollis Stål. (Hemiptera: Coreidae) is a key pest.1 Clavigralla tomentosicollis nymphs and adults cause high economic losses on cowpea by feeding on the pods.2 The damage is greater when the infestation occurs during flowering or pod-filling stage, and a treatment threshold is set at two to four larvae.3

Several control strategies, including cultural control methods and host plant resistance, have been explored with limited success.4 To date, the most effective control strategy relies on the spraying of synthetic insecticides. However, these pesticides are often not affordable to small-scale farmers and illiteracy can lead to their misuse which can generate many adverse effects.1 To find healthy and ecologically sustainable control method, our research has focused on biological control. Biological control of C. tomentosicollis using parasitoids has been less explored. Natural parasitism by the egg parasitoid Gryon fulviventre (Hymenoptera: Scelionidae) has been recorded on over 52% of the target insects in Nigeria and Burkina Faso.5,6

Natural parasitism by the egg parasitoid is low at the beginning of cowpea growing season but becomes high by the end of season leading to substantial reductions in the pest population.5,6 Although this observed high parasitism suggests a potential use of G. fulviventre to control C. tomentosicollis, to date, little attention has been given to this alternative control measure. Moreover, there is very little information on G. fulviventre’s bio-ecology and behavior.

The natural occurrence of parasitoids on a given pest does not necessarily make them effective biocontrol candidates. The selection of a parasitoid as a biological control agent relies on several requirements, including reproductive potential, effective mass rearing, and host-searching efficiency. Usually, parasitoid host searching is activated by a stimulus, such as complex volatiles from host insect and/or its host plant.7,8 In several parasitoid species, effective detection of this stimulus depends on the parasitoid’s ability to discriminate between a blend of volatiles produced both by herbivore-damaged plants and host insects.9,10 High host-searching efficiency is also known to be a key factor determining the success of several parasitoid species used in large-scale biological control attempts.1112-13

Sources of volatile compounds that may influence the parasitoid’s research behavior include the host plant (cowpea pods) and insect pest stages (particularly adults and eggs). Preliminary studies testing egg masses of C. tomentosicollis as volatiles source for females of G. fulviventre showed no significant host-searching behavior. Since then, in this study, we investigated the role of volatiles produced by cowpea pods and C. tomentosicollis adults on the host selection process of females from two strains of the parasitoid wasp G. fulviventre. The results could contribute to identify factors influencing host searching and to determine their importance in the implementation of a large-scale biological control strategy based on G. fulviventre.

Materials and Methods

Insect mass rearing

Strains of both C. tomentosicollis and G. fulviventre used in this study were derived from a laboratory mass rearing facility at the International Institute of Tropical Agriculture (IITA) in Cotonou, Benin. In the rearing room, the average temperature was 26.15°C ± 1.54°C and the mean relative humidity was 65.9% ± 7.6%. Clavigralla tomentosicollis nymphs and adults were supplied with fresh pods of a continuous crop of the sensitive Benin landrace cowpea variety, Kpodji-guê-guê, and were reared in cylindrical boxes (1900 mL each). Two strains (one from Burkina Faso and one from Benin) of the parasitoid G. fulviventre were reared on eggs of C. tomentosicollis. For this purpose, one mated G. fulviventre female was introduced in a cylindrical box (360 mL) for 48 hours with fifty fresh eggs of C. tomentosicollis. Emerging bug larvae hatching from nonparasitized eggs were removed from the box. The parasitized eggs were then monitored, and the subsequent generation of parasitoids emerged 16 days after parasitism occurred. Both strains of parasitoids were used in rearing and experiments as well.

For the olfactory tests, naive emerging G. fulviventre females were kept by pairs with males for mating prior to testing them. Burkina Faso and Benin are quite different in their climatic conditions which can influence insect ecology and behavior. That is the reason why both parasitoid strains were used in the hypothesis of a behavioral difference.

Obtaining the odors for olfactory tests

Several sources were used to obtain the tested odors. First of all, cowpea pods were collected from field at the IITA station. The harvested pods were previously washed with tap water to clean any other odor before use. The pods were placed under a stream of tap water for a few minutes without scrubbing to remove any insect odors that may be initially present. This does not change the structure of the pod and its odors and allows infestation with a controlled number of insects.

Infested pods were obtained by placing freshly harvested and cleaned pods with C. tomentosicollis adults and nymphs for 24 hours (24-hour infested pods) and 48 hours (48-hour infested pods). A total of five pods of each type were used for the experiment. Pods infested in this way for 48 hours are damaged enough to change the volatile compounds they emit. The healthy pods were not exposed to the insect prior to the trial. Three-day-old males and females of C. tomentosicollis collected from the rearing boxes were also used as source of odor. The insects used to produce odors were not provided with food over the course of the test.

Olfactometer setup

The response of G. fulviventre to volatiles produced by cowpea pods and C. tomentosicollis adults was investigated using a four-armed olfactometer previously described.14 This device was expected to determine the discriminatory ability of insects to more than two sources of odor at the same time. The device allows testing three different odors and one control at the same time as in a previous study.15 The four-armed olfactometer is a complex device that includes a central unit called the orientation chamber in which the insect can move freely. The chamber has four openings 90° apart that allow the entry of air. A hole which ensures the exit of the air is in the middle of the room. The latter is finally covered with a transparent glass plate. From the end to the orientation chamber, the olfactometer consists of a glass tube containing charcoal for the purification of air, another container of distilled water for humidifying the air, and four flowmeters that calibrate the air inlet. Each flowmeter was connected to an odor source (Figure 1). Clean airflow (wind speed: 300 mL/min) was divided into four subflows, and each subflow passed through one of the four odor sources connected to the four arms of the olfactometer. The device thus made it possible to deliver air loaded with each of the four test odors into the exposure chamber. The air exit hole in the middle of the orientation chamber prevents an accumulation of odors inside.

Figure 1.

Four-arm olfactometer device used for the different tests.

Picture: Apolline Sanou.

10.1177_1179543318825250-fig1.tif

Experimental procedure

Mated, three-day-old, naive G. fulviventre females (without any prior contact with cowpea pods or C. tomentosicollis adults) were introduced individually into the exposure chamber and their behavior was observed for a maximum of 5 minutes. Six sets of four-odor combinations (three odors and one control) were tested (Table 1). The choice of three, five, ten, and fifteen individuals of male and female for pheromone experiment was based on preliminary tests. The increasing number of individuals was expected to yield increasing amount of pheromone which affects parasitoid attraction.16 A test began once the female started moving, and the time spent in each odor field was recorded. Indirectly, the frequencies of entering in each odor field were recorded. Females remaining motionless for more than 2 minutes at the release point were discarded from the analysis. After testing five naive females, the positions of the odor sources were exchanged to correct for any potentially unforeseen asymmetry in the experimental setup. After testing ten naive female wasps, odor sources were renewed. In total, sixty naive female parasitoids from each strain were tested for each combination. Before each test, the arena was cleaned with laboratory alcohol. In the olfactometer room, the average temperature was 27.2°C and the mean relative humidity was 63.4%.

Table 1.

Details of experiments to determine the influence of volatiles produced by cowpea pods and Clavigralla tomentosicollis adults on the host location behavior of Gryon fulviventre females.

10.1177_1179543318825250-table1.tif

Data analysis

Data were analyzed to determine differences in the effect of the odor source on the behavior of female parasitoids. The Shapiro-Wilk and Levene tests in R (R Development Core Team 2014) were used to analyze the times spent by the parasitoids in each odor source to check for normality and homogeneity of variances, respectively. Several series of transformations (logx,log(x+1),x,(x+0.5),lnx,ln(x+1)) were also used without normalizing the data. So, the Kruskal-Wallis test, as an alternative to analysis of variance, was used with a = .05. Friedman tests17,18 with a = .05 were used to analyze the frequency of choice of G. fulviventre females for each of the odors tested using XLSTAT752 software (Addinsoft; XLSTAT752).

Results

Response of parasitoid females to odors from healthy and infested cowpea pods (Experiment 1)

The time spent by the parasitoids in the arms receiving odors from cowpea pods and the clean air ranged from 56 to 98 seconds for both strains of parasitoid (Burkina Faso and Benin). Females of both G. fulviventre strains were not significantly attracted by volatiles from either healthy or damaged cowpea pods (P = .495 and P = .558, respectively; Table 2). Similarly, mean frequencies of parasitoid choice among the 4 odors tested did not significantly differ for the Burkina Faso (P = .492) and Benin (P = .321) strains.

Table 2.

Response of both strains of Gryon fulviventre females to clean air and odors from healthy pods, 24-hour and 48-hour infested cowpea pods.

10.1177_1179543318825250-table2.tif

Response of parasitoid females to odors from Clavigralla tomentosicollis females (Experiment 2)

The parasitoid females were not significantly attracted by odors emitted by females of C. tomentosicollis (Table 3). Differences in time spent in the four arms of the olfactometer, as well as frequencies of choice between odors, did not significantly differ for both strains (Table 3).

Table 3.

Response of Gryon fulviventre females to clean air and odors from increasing number of Clavigralla tomentosicollis females.

10.1177_1179543318825250-table3.tif

Response of parasitoid females to odors from C. tomentosicollis males (Experiment 3)

Gryon fulviventre females were attracted by odors from males of C. tomentosicollis depending on not only the strain tested but also concentration (Table 4). For the Burkina Faso strain, the time spent by the parasitoids in the arm diffusing volatiles from C. tomentosicollis males was significantly different (P = .037), whereas the frequency of choice among the four odor sources did not differ (P > .05). For the Benin strain, only the frequency of choice of G. fulviventre females for the odors from C. tomentosicollis males was significantly different (P = .001).

Table 4.

Response of Gryon fulviventre females to clean air and odors from increasing numbers of Clavigralla tomentosicollis males.

10.1177_1179543318825250-table4.tif

Discriminatory response of parasitoid females between combined odors from healthy pods, infested pods, and C. tomentosicollis males (Experiments 4-6)

As the compounds released by males of C. tomentosicollis attracted G. fulviventre females, we also tested their response to odors from an increasing number of males in comparison with volatiles from healthy and infested cowpea pods (Tables 5 to 7).

Table 5.

Discriminatory response of Gryon fulviventre females to volatiles from cowpea pods and five males of Clavigralla tomentosicollis.

10.1177_1179543318825250-table5.tif

Table 6.

Discriminatory response of Gryon fulviventre females to volatiles from cowpea pods and ten males of Clavigralla tomentosicollis.

10.1177_1179543318825250-table6.tif

Table 7.

Response of Gryon fulviventre females to discriminate volatiles from cowpea pods and fifteen males of Clavigralla tomentosicollis.

10.1177_1179543318825250-table7.tif

Females of both strains showed no significant difference for the time spent or the frequency of choice for the odor sources tested with five males (Table 5). However, females were attracted by the odors released by ten males of C. tomentosicollis as evidenced by the higher frequencies of choice in Burkina Faso strain (P = .028). Females in Benin strain showed a discriminatory capacity of the different odors (P = .008), but they did not discriminate odors between infested pods and ten males (Table 6). Again parasitoid females of both strains were not significantly attracted when the tested odors were provided by cowpea pods and 15 C. tomentosicollis males (Table 7).

Discussion

This study demonstrated that olfactory stimuli are used by G. fulviventre females to locate their host C. tomentosicollis. However, the parasitoid females did not discriminate between volatiles produced by healthy and infested cowpea pods when they were exposed only to cowpea volatiles. For many parasitoid species, pest-damaged plants, including maize19 and soybean,20,21 release substances used as synomones by parasitoids to locate the pest-hosts. Our result suggests, in contrast to other parasitoid species, that G. fulviventre females do not use volatiles from cowpea pods damaged by C. tomentosicollis to detect the presence of its host making this kind of indirect plant species defense against pests18 unavailable to Vigna unguiculata.

Previous studies demonstrated that some parasitoid species use their host’s pheromones to locate host presence.22232425-26 We hypothesize that G. fulviventre may be attracted either to a sexual pheromone used by C. tomentosicollis males to attract females or an aggregation pheromone released by the males. Such an assumption is based on previous observations indicating the possibility for parasitoids to use host-male insect’s pheromones as kairomones to locate the hosts.27282930-31

However, the results suggest that this odor attractiveness effect could depend on the number of C. tomentosicollis males used. At low and high densities (five and fifteen individuals, respectively), G. fulviventre females did not discriminate odors from the males. This finding suggests, on one hand, that a minimal amount of pheromone is first needed to trigger a response in parasitoids and that, on the other hand, the amount of pheromone released may in some way decrease once the pest densities have exceeded a certain threshold. Moreover, simply due to their regrouping in the olfactometer and regulating their density, the insects can inhibit the secretion of the congeners’ attractive pheromone.3233-34 Such inhibition involves the secretion of anti-aggregation substances,33,35 which would not be perceived by the parasitoid or which would not play an attractive role for G. fulviventre female. Otherwise, pheromone is a mixture of several compounds and some of the compounds would act as a repellent for parasitoids.36,37 An experimental olfactometer offers small and confined space distinct from real environmental conditions. Further experiments in actual environmental conditions could better establish what pest density, if any, triggers parasitoid infestation. Moreover, the precise identification of attractants for female parasitoids is an important step in considering the release of such substances to attract more parasitoids at the right time to prevent the growth of pest populations. In the wild, visual stimuli can also be involved, with or without olfactory signals, in triggering parasitoid activities.383940-41 Any role of this for host location behavior in G. fulviventre remains to be investigated. Provided that a precise attractive mechanism is characterized to ensure parasitism, then mass rearing and release of G. fulviventre at the beginning of the growing season when pest infestation initially occurs could potentially be used to control C. tomentosicollis populations.

Conclusions

The results obtained from this study are of great importance in the understanding of host-parasitoid interactions using a model that has been poorly studied, such as the egg parasitoid G. fulviventre and the major cowpea pod-sucking bug pest, C. tomentosicollis. The main findings indicated that the parasitoid females are attracted by olfactory cues provided by the males of their host species alone, cowpea pods (infested or not) being not attractive. Although precise determination of attractive volatile compounds emitted by C. tomentosicollis males remains for future research, the attractiveness of the involved compound depended on the density of males present and probably on the dose of volatiles produced. Subsequent studies could also characterize any role of other factors influencing the biological potential of this control agent, a necessary step for developing a best practice strategy for an effective protection of cowpea fields in West Africa.

Acknowledgements

The authors are grateful to the International Institute of Tropical Agriculture (IITA) in Cotonou, Benin, for technical assistance and research facilities.

REFERENCES

1.

Dabiré CL Tignegré JB Ba NM. An historical review of progress to control key cowpea biotic constraints in Burkina Faso. Paper presented at: Proceedings of the Fifth World Cowpea Conference on Improving Livelihoods in the Cowpea Value Chain through Advancement in Science: Innovative Research along the Cowpea Value Chain; September 27-October 1, 2012; Ibadan, Nigeria. Google Scholar

2.

Dabiré CL Kini F Ba NM Dabire R Fouabi K. Effet du stade de développement des gousses de niébé sur la biologie de la punaise suceuse Clavigralla tomentosicollis (Hemiptera: Coreidae). Int J Trop Insect Sci. 2005;25:25–31. Google Scholar

3.

Jackai LEN Atropo PK Odebiy JA . Use of the response of two growth stages of cowpea to different population densities of the coreid bug, Clavigralla tomentosicollis (Stål.) to determine action threshold levels. Crop Protect. 1989;8:422–428. Google Scholar

4.

Ba NM Sawadogo F Dabire-Binso CL Drabo I Sanon A. Insecticidal activity of three plants extracts on the cowpea pod sucking bug, Clavigralla tomentosicollis, STÄL (Hemiptera: Coreidae). Pak J Biol Sci. 2009;12:1320–1324. Google Scholar

5.

Asante SK Jackai LE Tamo M. Efficiency of Gryon fulviventris (Hymenoptera: Scelionidae) as an egg parasitoid of Clavigralla tomentosicollis (Hemiptera: Coreidae) in northern Nigeria. Environ Entomol. 2000;29:815–821. Google Scholar

6.

Dabiré CL. Etude de quelques parametres biologiques et écologiques de Clavigralla tomentosicollis Stäl 1855 (Hemiptera: Coreidae), punaise suceuse des gousses de niébé [Vigna unguiculata (L.) Walp.] dans une perspective de lutte durable contre l’insecte au Burkina Faso [PhD dissertation]. Abidjan, Côte d’Ivoire: Université de Cocody; 2001:169. Google Scholar

7.

Conti E Colazza S. Chemical ecology of egg parasitoids associated with true bugs. Psyche. 2012;2012:651015. Google Scholar

8.

Fatouros NE Dicke M Mumm R Meiners T Hilker M. Foraging behavior of egg parasitoids exploiting chemical information. Behav Ecol. 2008;19:677–689. Google Scholar

9.

Dicke M . Evolution of induced indirect defense of plants. In: Tollrian R Harvell C , ed. The Ecology and Evolution of Inducible Defenses. Princeton, NJ: Princeton University Press; 1999:62–88. Google Scholar

10.

Turlings TC Tumlinson JH Heath RR Proveaux AT Doolittle RE. Isolation and identification of allelochemicals that attract the larval parasitoid, Cotesia marginiventris (Cresson), to the microhabitat of one of its hosts. J Chem Ecol. 1991;17:2235–2251. Google Scholar

11.

Gross P Hawkins BA Cornell HV Hosmane B. Using lower trophic level factors to predict outcomes in classical biological control of insect pests. Basic Appl Ecol. 2005;6:571–584. Google Scholar

12.

Ngi-Song AJ Overholt WA. Host location and acceptance by Cotesia flavipes Cameron and C. sesamiae (Cameron) (Hymenoptera: Braconidae), parasitoids of African gramineous stemborers: role of Frass and other host cues. Biol Control. 1997;9:136–142. Google Scholar

13.

Vet LE. Parasitoid searching efficiency links behaviour to population processes. Appl Entomol Zool. 2001;36:399–408. Google Scholar

14.

Vet LE Lenteren JV Heymans M Meelis E. An airflow olfactometer for measuring olfactory responses of hymenopterous parasitoids and other small insects. Physiol Entomol. 1983;8:97–106. Google Scholar

15.

Atachi P Hountondji FCC . Olfactory responses of Maruca vitrata (Fabricius) larvae to reproductive parts of different varieties of cowpea, Vigna unguiculata (L.) Walp. Int J Trop Insect Sci. 2000;20:117–121. Google Scholar

16.

Branco M Jactel H Franco JC Mendel Z. Modelling response of insect trap captures to pheromone dose. Ecol Model. 2006;197:247–257. Google Scholar

17.

Friedman M. The use of ranks to avoid the assumption of normality implicit in the analysis of variance. J Am Stat Assoc. 1937;32:675–701. Google Scholar

18.

Friedman M. A comparison of alternative tests of significance for the problem of m rankings. Ann Math Statist. 1940;11:86–92. Google Scholar

19.

Rasmann S Turlings TC. Simultaneous feeding by aboveground and belowground herbivores attenuates plant-mediated attraction of their respective natural enemies. Ecol Lett. 2007;10:926–936. Google Scholar

20.

Moraes MC Pareja M Laumann RA Hoffmann-Campo CB Borges M. Response of the parasitoid Telenomus podisi to induced volatiles from soybean damaged by stink bug herbivory and oviposition. J Plant Interact. 2008;3:111–118. Google Scholar

21.

D’Alessandro M Brunner V von Mérey G Turlings TC. Strong attraction of the parasitoid Cotesia marginiventris towards minor volatile compounds of maize. J Chem Ecol. 2009;35:999–1008. doi: https://doi.org/10.1007/s10886-009-9692-7. Google Scholar

22.

Dannon EA Tamò M Van Huis A Dicke M. Effects of volatiles from Maruca vitrata larvae and caterpillar-infested flowers of their host plant Vigna unguiculata on the foraging behavior of the parasitoid Apanteles taragamae. J Chem Ecol. 2010;36:1083–1091. Google Scholar

23.

Colazza S Salerno G Wajnberg E. Volatile contact chemicals released by Nezara viridula (Heteroptera: Pentatomidae) have a kairomonal effect on the egg parasitoid Trissolcus basalis (Hymenoptera: Scelionidae). Biol Control. 1999;16:310–317. Google Scholar

24.

Silva CC Moraes MCB Laumann RA Borges M. Sensory response of the egg parasitoid Telenomus podisi to stimuli from the bug Euschistus heros. Pesq Agrop Bras. 2006;41:1093–1098. Google Scholar

25.

Son JK Choo HY Choi JY Paik CH Park CG. Enhancement of Riptortus clavatus (Thunberg) (Hemiptera: Alydidae) egg parasitism by a component of the bug’s aggregation pheromone. J Asia Pac Entomol. 2009;12:159–163. Google Scholar

26.

Yasuda K. Function of the male pheromone of the leaf-footed plant bug, Leptoglossus australis (Fabricius) (Heteroptera: Coreidae) and its kairomonal effect. Jpn Agri Res Quart. 1998;32:161–165. Google Scholar

27.

Blatt SE Borden JH. Evidence for a male-produced aggregation pheromone in the western conifer seed bug, Leptoglossus occidentalis Heidemann (Hemiptera: Coreidae). Can Entomol. 1996;128:777–778. Google Scholar

28.

Lopez S Quero C Iturrondobeitia JC Guerrero A Goldarazena A. Evidence for (E) pityol as an aggregation pheromone of Pityophthorus pubescens (Coleoptera: Curculionidae: Scolytinae). Can Entomol. 2011;143:447–454. Google Scholar

29.

Soldi RA Rodrigues MA Aldrich JR Zarbin PH. The male-produced sex pheromone of the true bug, Phthia picta, is an unusual hydrocarbon. J Chem Ecol. 2012;38:814–824. Google Scholar

30.

Wang Q Millar JG. Mating behavior and evidence for male-produced sex pheromones in Leptoglossus clypealis (Heteroptera: Coreidae). Ann Entomol Soc Am. 2000;93:972–976. Google Scholar

31.

Yasuda K Tsurumachi M. Influence of male adults of the leaf-footed bug Leptoglossus australis (Fabricius) (Heteroptera: Coreidae) on host-searching of the egg parasitoïd Gryon pennsylvanicum (Ashmead). Appl Entomol Zool. 1995;30:139–144. Google Scholar

32.

Byers JA. Chemical ecology of bark beetles. Experientia. 1989;45:271–283. Google Scholar

33.

Byers JA Wood DL Craig J Hendry LB. Attractive and inhibitory pheromones produced in the bark beetle, Dendroctonus brevicomis, during host colonization: regulation of inter-and intraspecific competition. J Chem Ecol. 1984;10:861–877. Google Scholar

34.

Wertheim B van Baalen EJA Dicke M Vet LE. Pheromone-mediated aggregation in nonsocial arthropods: an evolutionary ecological perspective. Annu Rev Entomol. 2005;50:321–346. Google Scholar

35.

Blomquist GJ Figueroa-Teran R Aw Met al . Pheromone production in bark beetles. Insect Biochem Mol Biol. 2010;40:699–712. Google Scholar

36.

Roh GH Kim J Park CG. Possible antagonism of (Z)-2-hexenyl (E)-3-hexenoate against the attractiveness of (E)-2-hexenyl (Z)-3-hexenoate to Ooencyrtus nezarae (Hymenoptera: Encyrtidae). J Appl Entomol. 2018;142:327–332. Google Scholar

37.

Zhong YZ Zhang JP Ren LLet al . Behavioral responses of the egg parasitoid Trissolcus japonicus to volatiles from adults of its stink bug host, Halyomorpha halys. J Pest Sci. 2017;90:1097–1105. Google Scholar

38.

Bell WJ. Searching Behaviour: The Behavioural Ecology of Finding Resources. Berlin, Germany: Springer; 2012. Google Scholar

39.

Brévault T Quilici S. Interaction between visual and olfactory cues during host finding in the tomato fruit fly Neoceratitis cyanescens. J Chem Ecol. 2010;36:249–259. Google Scholar

40.

Houot B Gigot V Robichon A Ferveur JF. Free flight odor tracking in Drosophila: effect of wing chemosensors, sex and pheromonal gene regulation. Sci Rep. 2017;7:40221. Google Scholar

41.

Luo CW Chen Y. Phototactic behavior of Scleroderma guani (Hymenoptera: Bethylidae)-parasitoid of Pissodes punctatus (Coleoptera: Curculionidae). J Insect Behav. 2016;29:605–614. Google Scholar

Notes

[1] Financial disclosure The author(s) disclosed receipt of the following financial support for the research, authorship and/or publication of this article: This study has been supported by the Legumes Innovation Lab, formerly known as the Dry Grain Pulses Collaborative Research Support Program (CRSP), by the Bureau for Economic Growth, Agriculture, and Trade, US Agency for International Development, under the terms of grant no. EDH-A-00-07-00005.

[2] Conflicts of interest The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

[3] Contributed by The research was conducted by ApS under the supervision of mentors listed as co-authors. All co-authors participated in defining the research methodology and writing/editing the paper.

© The Author(s) 2019 This article is distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 License (http://www.creativecommons.org/licenses/by-nc/4.0/) which permits non-commercial use, reproduction and distribution of the work without further permission provided the original work is attributed as specified on the SAGE and Open Access pages (https://us.sagepub.com/en-us/nam/open-access-at-sage).
Apolline Sanou, Fousséni Traoré, Malick Niango Ba, Clémentine L Dabiré-Binso, Barry R Pittendrigh, and Antoine Sanon "Effects of Volatiles from Clavigralla tomentosicollis Stål. (Hemiptera: Coreidae) Adults on the Host Location Behavior of the Egg Parasitoid Gryon fulviventre (Crawford) (Hymenoptera: Scelionidae)," International Journal of Insect Science 11(1), (1 January 2020). https://doi.org/10.1177/1179543318825250
Received: 8 December 2018; Accepted: 17 December 2018; Published: 1 January 2020
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