Electroantennogram response of the parasitoid, <i>Microplitis croceipes</i> to host-related odors: The discrepancy between relative abundance and level of antennal responses to volatile compound

Tolulope Morawo; Matthew Burrows; Henry Fadamiro

doi:10.12688/f1000research.10104.2

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Research Note

Revised

Electroantennogram response of the parasitoid, Microplitis croceipes to host-related odors: The discrepancy between relative abundance and level of antennal responses to volatile compound

[version 2; peer review: 4 approved]

Tolulope Morawo ¹, Matthew Burrows^1,2, Henry Fadamiro¹

PUBLISHED 09 Mar 2017

Author details Author details

¹ Department of Entomology & Plant Pathology, Auburn University, Auburn, USA
² Division of Parasitic Diseases and Malaria- Entomology, Centers for Disease Control and Prevention, Atlanta, USA

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Abstract

Herbivores emit volatile organic compounds (VOCs) after feeding on plants. Parasitoids exploit these VOCs as odor cues to locate their hosts. In nature, host-related odors are emitted as blends of various compounds occurring in different proportions, and minor blend components can sometimes have profound effects on parasitoid responses. In a previous related study, we identified and quantified VOCs emitted by cotton plant-fed Heliothis virescens (Lepidoptera: Noctuidae) larvae, an herbivore host of the parasitoid Microplitis croceipes (Hymenoptera: Braconidae). In the present study, the olfactory response of female M. croceipes to synthetic versions of 15 previously identified compounds was tested in electroantennogram (EAG) bioassays. Using M. croceipes as a model species, we further asked the question: does the relative abundance of a volatile compound match the level of antennal response in parasitoids? Female M. croceipes showed varying EAG responses to test compounds, indicating different levels of bioactivity in the insect antenna. Eight compounds, including decanal, 1-octen-3-ol, 3-octanone, 2-ethylhexanol, tridecane, tetradecane, α-farnesene and bisabolene, elicited EAG responses above or equal to the 50^th percentile rank of all responses. Interestingly, decanal, which represented only 1% of the total amount of odors emitted by cotton-fed hosts, elicited the highest (0.82 mV) EAG response in parasitoids. On the other hand, (E)-β-caryophyllene, the most abundant (29%) blend component, elicited a relatively low (0.17 mV) EAG response. The results suggest that EAG response to host-related volatiles in parasitoids is probably more influenced by the ecological relevance or functional role of the compound in the blend, rather than its relative abundance.

Keywords

Braconidae, endoparasitoid, Heliothis virescens, cotton plant

Corresponding author: Tolulope Morawo

Competing interests: No competing interests were disclosed.

Grant information: The author(s) declared that no grants were involved in supporting this work.

Copyright: © 2017 Morawo T et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Data associated with the article are available under the terms of the Creative Commons Zero "No rights reserved" data waiver (CC0 1.0 Public domain dedication).

How to cite: Morawo T, Burrows M and Fadamiro H. Electroantennogram response of the parasitoid, Microplitis croceipes to host-related odors: The discrepancy between relative abundance and level of antennal responses to volatile compound [version 2; peer review: 4 approved]. F1000Research 2017, 5:2725 (https://doi.org/10.12688/f1000research.10104.2) First published: 21 Nov 2016, 5:2725 (https://doi.org/10.12688/f1000research.10104.1) Latest published: 09 Mar 2017, 5:2725 (https://doi.org/10.12688/f1000research.10104.2)

Revised Amendments from Version 1

General comment: We thank all the referees for the important comments they provided while reviewing this manuscript. In several instances, we made appropriate changes to the new version according to the suggestions of the referees. In a few other areas, we have avoided the inclusion of information that is beyond the scope of the study so as to keep the article focused and concise. As clearly stated, the present study builds on the results of a previous study by the authors.

Introduction: We added a few sentences to better introduce the concept of plant-associated odors emitted by cotton-fed larvae. We clarified that odors emitted from plants play a key role in the location of host patch by parasitoids, and that odors emitted by plant-fed herbivores may be more useful in short-range host location. Finally, we added some more details about the results of the previous study conducted by the authors to create a better background for the present study.

Materials and methods: We have included justification for the mass/volume concentration used to formulate the synthetic compounds and the single dose used in EAG recordings. Furthermore, we clarified the arrangement used to present compounds to each insect replicate. We also clarified that parasitoids used in EAG recordings were reared on host larvae that fed on artificial diet so that their sensitivity to plant odors will not be biased.

Results: EAG response to solvent control was not shown because the data represent absolute EAG, in which the response to control has been deducted from responses to treatment compounds. The dataset is available for review.

Discussion: The suggested citation by one of the referees has been added to the discussion. Also, we added a statement to note that parasitoids can learn to respond to diverse odor cues.

To read any peer review reports and author responses for this article, follow the "read" links in the Open Peer Review table.

Introduction

Infested plants emit volatile organic compounds (VOCs) as an indirect defense against herbivore damage^1,2. Informative volatile cues used by parasitoids for host location can be emitted by plants infested with herbivores^1,2 or emitted by herbivores that fed on plants^3,4. Although plant volatiles may initially lead parasitoids to the host patch, herbivore host-specific odors are important short-range cues used in the later stages of host location⁵. The specific mechanism by which plant-fed host larvae emit these volatiles is not fully understood. However, it is evident that parasitoids use these plant-associated VOCs in the host location process⁵. Such odor cues are usually released as a blend of various compounds in nature. Consequently, differentiating useful cues from ecologically irrelevant odors can be challenging for foraging parasitoids. Therefore, it is expected that antennal sensitivity of parasitoids will vary in response to different compounds. Antenna sensitivity in insects can be measured with electroantennogram (EAG) recording. EAG measures the summed activity of olfactory receptor neurons in the antenna and indicates the level of biological activity elicited by various compounds.

Microplitis croceipes (Hymenoptera: Braconidae) is an endoparasitoid of Heliothis virescens (Lepidoptera: Noctuidae), which is an important pest of cotton plant. In a previous related study⁵, female M. croceipes showed attraction to the odor blend emitted by cotton-fed H. virescens larvae in Y-tube olfactometer bioassays⁵. The blend components were identified and quantified using gas chromatography-mass spectrometry (GC/MS). Furthermore, the compounds in the attractive blend occurred in varying proportions (Table 1). However, the relative abundance of a blend component does not necessarily indicate its relevance to resource location in insects⁶. In the present study, olfactory response of M. croceipes to synthetic versions of 15 previously identified compounds was tested in EAG bioassays. Comparing EAG results in the present study and GC/MS analyses in a previous study⁵, we indicated the discrepancy between relative abundance of a volatile blend component and the level of antennal response in parasitoids.

Table 1. Composition of headspace volatile organic compounds emitted by cotton-fed Heliothis virescens larvae.

This table was modified from Morawo and Fadamiro (doi: 10.1007/s10886-016-0779-7)⁵, with permission from the authors.

ID¹	Compound	Relative abundance (%)	Chemical category
1	α-Pinene	15.1	Monoterpene
2	β-Pinene	1.6	Monoterpene
3	1-Octen-3-ol	1.4	Alcohol
4	3-Octanone	0.8	Ketone
5	Myrcene	2.7	Monoterpene
6	Unknown²	1.2	-
7	Limonene	9.1	Monoterpene
8	2-Ethylhexanol	2.2	Alcohol
9	Decanal	1.0	Aldehyde
10	Tridecane	6.2	Alkane
11	Tetradecane	2.4	Alkane
12	(E)-β-Caryophyllene	29.2	Sesquiterpene
13	α-Bergamotene²	0.7	Sesquiterpene
14	α-Humulene	6.5	Sesquiterpene
15	α-Farnesene	0.8	Sesquiterpene
16	Bisabolene	8.6	Sesquiterpene
17	α-Bisabolol	7.9	Sesquiterpene

¹In order of elution during gas chromatography.

²Compounds that were not tested in the present study.

Methods and materials

Insects

Microplitis croceipes was reared on 2^nd–3^rd instar larvae of Heliothis virescens. The larvae of H. virescens used to rear M. croceipes were fed pinto bean artificial diet. Thus, parasitoids had no experience with plant odors. Adult wasps were supplied with 10% sugar water upon emergence in our laboratory at Entomology & Plant Pathology Department, Auburn University. For more details about rearing protocol, see Lewis and Burton⁷. Female parasitoids used for EAG bioassays were 2–3 days-old, presumed mated (after at least 24 h of interaction with males), and inexperienced with oviposition or plant material. The general rearing conditions for all insects were 25±1 °C, 75±5 % relative humidity and 14:10 h (light:dark) photoperiod.

EAG recording

EAG responses of M. croceipes to 15 synthetic compounds (Table 1), previously identified in the headspace of cotton-fed H. virescens larvae⁵, were recorded according to the method described by Ngumbi et al.⁸ with modifications. Two compounds, α-bergamotene (not commercially available) and an unidentified compound reported in the previous study⁵ were not tested in the present study. α-Pinene, β-pinene, myrcene, limonene, 2-ethylhexanol, tridecane, (E)-β-caryophyllene, α-humulene, α-farnesene and α-bisabolol with purity 95–99% were purchased from Sigma-Aldrich^® (St. Louis, MO, USA). 1-Octen-3-ol, 3-octanone, decanal, tetradecane and bisabolene with purity 96–99% were purchased from Alfa Aesar^® (Ward Hill, MA, USA). Test compounds were formulated in hexane at 0.1 μg/μl and delivered onto Whatman^®No.1 filter paper strips at an optimum dose of 1 µg. Mass/volume concentration was used to correct for differences in purity of synthetic compounds. The dose was selected as ecologically relevant based on GC/MS analyses results of total amount of volatiles emitted by cotton-fed H. virescens larvae⁵. Impregnated filter papers were placed inside glass Pasteur pipettes and stimulus was introduced as 0.2 s odor puffs. A glass capillary reference electrode filled with 0.1 M KCl was attached to the back of the wasp head, and a similar recording electrode was connected to the excised tip of the wasp antenna. The analog signal was detected through a probe and processed with a data acquisition controller (IDAC-4, Syntech, The Netherlands). Data was assessed using EAG 2000 software (Syntech, The Netherlands). EAG responses to the 15 compounds and control (hexane) were sequentially recorded for each of 15 insect replicates. Each compound was presented at positions 1 through 15 across replicates to minimize positional bias. For instance, 1-octen-3-ol and 3-octanone were introduced to the first insect as the 3^rd and 4^th compounds, respectively, but introduced to the second insect as the 4^th and 5^th compounds, respectively.

Data analyses

Differences in absolute EAG values (EAG response to compound minus response to solvent control) of synthetic compounds were analyzed using the Kruskal-Wallis test, followed by Sidak’s multiple comparison test. The relationship between EAG response and relative abundance was analyzed with Proc Corr (correlation) procedure in SAS. All analyses were performed in SAS v9.2 (SAS Institute Inc., Cary, NC, USA) with P=0.05 level of significance.

Results

Female M. croceipes showed varying EAG responses to test compounds (range: 0.05–0.82 mV; Figure 1). Decanal elicited the highest EAG response (0.82 mV; χ2 = 134.13; df = 14; P<0.0001), while β-pinene elicited the lowest response (0.05 mV) in parasitoids. Decanal, tridecane, 3-octanone, 2-ethylhexanol, 1-octen-3-ol, bisabolene, tetradecane and α-farnesene elicited EAG responses ≥0.22 mV (50^th percentile rank). Four of the top bioactive compounds: decanal, 3-octanone, 1-octen-3-ol and 2-ethylhexanol were emitted in quantities ≤2.2% of the total blend (Table 1). On the other hand, (E)-β-caryophyllene, the most abundant (29.2% of total blend) component, elicited a relatively low EAG response (0.17 mV) in parasitoids (Figure 1). However, the negative correlation between EAG response and relative abundance of compounds was not statistically significant (r = -0.33; N = 15; P=0.23).

Figure 1. EAG responses of Microplitis croceipes to synthetic compounds.

Mean absolute Electroantennogram (EAG) responses (mV ± SEM; N = 15) of female Microplitis croceipes to 15 volatile compounds identified in the headspace of cotton-fed Heliothis virescens larvae⁵. Synthetic compounds were formulated in hexane (solvent control) and tested at an optimum dose of 1 μg. Orange line indicates the arbitrary response threshold of 0.22 mV (50^th percentile rank). Bars with no letters in common are significantly different (P<0.05; Kruskal-Wallis test followed by Sidak’s multiple comparison test).

Compounds tested								EAG response (mV)
	Rep 1	Rep 2	Rep 3	Rep 4	Rep 5	Rep 6	Rep 7	Rep 8	Rep 9	Rep 10	Rep 11	Rep 12	Rep 13	Rep 14	Rep 15

Hexane (control 1)	0.072	0.165	0.056	0.178	0.093	0.157	0.081	0.053	0.099	0.096	0.05	0.26	0.156	0.063	0.118

Alpha-Pinene	0.224	0.129	0.181	0.151	0.215	0.075	0.181	0.255	0.108	0.102	0.133	0.229	0.118	0.118	0.202
Beta-Pinene	0.13	0.235	0.096	0.072	0.151	0.035	0.169	0.154	0.047	0.087	0.062	0.329	0.118	0.078	0.158
1-Octen-3-ol	0.486	0.472	0.413	0.258	0.761	0.181	0.672	0.694	0.169	0.191	0.255	0.437	0.357	0.266	0.368
3-Octanone	0.502	0.484	0.496	0.496	0.514	0.166	0.676	0.761	0.169	0.188	0.228	0.566	0.469	0.22	0.498
Myrcene	0.23	0.283	0.166	0.325	0.209	0.069	0.313	0.31	0.047	0.123	0.1	0.204	0.181	0.089	0.138
Limonene	0.136	0.15	0.066	0.224	0.355	0.169	0.148	0.322	0.035	0.066	0.127	0.097	0.152	0.097	0.339
2-Ethylhexanol	0.389	0.621	0.416	0.788	0.752	0.633	0.355	0.508	0.145	0.041	0.178	0.441	0.432	0.217	0.403
Decanal	1.188	0.868	1.057	1.182	1.667	0.996	1.197	1.276	0.337	0.807	0.455	0.599	0.774	0.355	0.736
Tridecane	0.425	0.519	0.459	0.465	0.547	0.45	0.514	0.657	0.761	0.184	0.228	0.542	0.418	0.213	0.418
Tetradecane	0.212	0.405	0.355	0.428	0.529	0.288	0.401	0.52	0.566	0.276	0.133	0.275	0.368	0.149	0.382
(E)-Beta-Caryophyllene	0.203	0.155	0.306	0.288	0.465	0.23	0.395	0.377	0.242	0.12	0.155	0.318	0.214	0.069	0.235
Alpha-Humulene	0.12	0.153	0.203	0.184	0.316	0.123	0.227	0.377	0.163	0.133	0.095	0.228	0.191	0.052	0.339
Alpha-Farnesene	0.191	0.208	0.264	0.331	0.502	0.206	0.413	0.599	0.273	0.166	0.248	0.339	0.316	0.086	0.359
Bisabolene	0.2	0.266	0.422	0.252	0.374	0.239	0.453	0.602	0.297	0.313	0.249	0.62	0.319	0.289	0.556
Alpha-Bisabolol	0.066	0.118	0.148	0.114	0.267	0.062	0.178	0.3	0.066	0.084	0.072	0.127	0.1	0.103	0.219

Hexane (control 2)	0.017	0.059	0.084	0.066	0.081	0.012	0.096	0.099	0.029	0.023	0.031	0.097	0.03	0.021	0.083




Correlation data
Compound	Rel. Amt (%)	Absolute EAG (mV)
Alpha-Pinene	15.1	0.077866667
Beta-Pinene	1.6	0.051666667
1-Octen-3-ol	1.4	0.3145
3-Octanone	0.8	0.3447
Myrcene	2.7	0.1038
Limonene	9.1	0.089
2-Ethylhexanol	2.2	0.338333333
Decanal	1	0.815433333
Tridecane	6.2	0.369166667
Tetradecane	2.4	0.2683
(E)-Beta-Caryophyllene	29.2	0.1673
Alpha-Humulene	6.5	0.109433333
Alpha-Farnesene	0.8	0.2159
Bisabolene	8.6	0.279233333

Dataset 1.EAG responses of Microplitis croceipes to synthetic compounds and correlation with relative abundance of compounds.

Discussion

EAG responses of Micropiltis croceipes in the present study indicated variation in biological activity elicited by test compounds at the peripheral level, and revealed a discrepancy between relative abundance and level of antennal responses in parasitoids. High EAG response elicited by decanal in M. croceipes agrees with previous reports on olfactory responses of the parasitoids, Microplitis mediator⁹ and Bracon hebetor¹⁰. Furthermore, decanal is a key attractant for host-seeking M. croceipes⁵. Although compounds are emitted in different quantities in natural blends, minor components can have a profound effect on resource location in parasitoids^6,11. Interestingly, decanal constituted only 1% of the total blend emitted by cotton-fed H. virescens⁵, but elicited the highest EAG response in M. croceipes, supporting the “little peaks-big effects” concept⁶. On the other hand, (E)-β-caryophyllene, the most abundant blend component, elicited a relatively low EAG response in parasitoids.

Therefore, it is more likely that the ecological relevance of a compound, rather than its relative abundance determines the level of olfactory response in foraging insects. For instance, small amounts of isothiocyanates in the volatile blend of brassica plants serve as host location cues for parasitoids of brassica herbivores^12,13. More importantly, blend components act in concert to provide parasitoids with complete information¹⁴. Consequently, certain compounds function as background odors to enhance detectability (olfactory contrast) of other attractive components in a blend^12,15. It is possible that (E)-β-caryophyllene serves as a background odor in the blend emitted by cotton-fed H. virescens. Finally, it should be noted that while EAG measures the level of bioactivity, behavioral bioassays are usually needed to establish the functional role of various compounds^5,16. In addition, several species of parasitoids can be conditioned to respond to diverse odor cues, regardless of the relevance of such odor cues to their ecology.

Data availability

Dataset 1. EAG responses of Microplitis croceipes to synthetic compounds and correlation with relative abundance of compounds. Electroantennogram (EAG) data shows actual EAG response readouts to different compounds for 15 insect replicates. Absolute EAG value for each compound in a replicate can be obtained by deducting the average of two controls (Control 1 and Control 2) from the actual EAG values. Correlation data shows relative abundance of 15 blend components and their corresponding mean absolute EAG values. Details of data analyses were indicated in the main text and Figure 1 legend. Raw data behind the representation shown in Figure 1 and analyses referred to in the Results section are included. DOI: 10.5256/f1000research.10104.d143446¹⁷.

Author contributions

TM and HF conceived the study. TM designed the experiment. TM and MB carried out the research. All authors contributed to writing and revision of the manuscript.

Competing interests

No competing interests were disclosed.

Grant information

The author(s) declared that no grants were involved in supporting this work.

Acknowledgements

We thank Brandice Kopishke for rearing the insects used for this study.

Faculty Opinions recommended

References

1. De Moraes CM, Lewis WJ, Paré PW, et al.: Herbivore-infested plants selectively attract parasitoids. Nature. 1998; 393: 570–573. Publisher Full Text
2. Turlings TC, Wäckers F: Recruitment of predators and parasitoids by herbivore-injured plants. Adv Insect Chem Ecol. 2004; 2: 21–75. Reference Source
3. de Rijk M, Krijn M, Jenniskens W, et al.: Flexible parasitoid behaviour overcomes constraint resulting from position of host and nonhost herbivores. Anim Behav. 2016; 113: 125–135. Publisher Full Text
4. Elzen GW, Williams HJ, Vinson SB: Role of diet in host selection of Heliothis virescens by parasitoid Campoletis sonorensis (Hymenoptera: Ichneumonidae). J Chem Ecol. 1984; 10: 1535–1541. Publisher Full Text
5. Morawo T, Fadamiro H: Identification of key plant-associated volatiles emitted by Heliothis virescens larvae that attract the parasitoid, Microplitis croceipes: implications for parasitoid perception of odor blends. J Chem Ecol. 2016; 1–10. PubMed Abstract | Publisher Full Text
6. Clavijo McCormick A, Gershenzon J, Unsicker SB: Little peaks with big effects: establishing the role of minor plant volatiles in plant-insect interactions. Plant Cell Environ. 2014; 37(8): 1836–1844. PubMed Abstract | Publisher Full Text
7. Lewis WJ, Burton RL: Rearing Microplitis croceipes in the laboratory with Heliothis zea as host. J Econ Entomol. 1970; 63(2): 656–658. Publisher Full Text
8. Ngumbi E, Chen L, Fadamiro H: Electroantennogram (EAG) responses of Microplitis croceipes and Cotesia marginiventris and their lepidopteran hosts to a wide array of odor stimuli: correlation between EAG response and degree of host specificity? J Insect Physiol. 2010; 56(9): 1260–1268. PubMed Abstract | Publisher Full Text
9. Yu H, Zhang Y, Wyckhuys KA, et al.: Electrophysiological and behavioral responses of Microplitis mediator (Hymenoptera: Braconidae) to caterpillar-induced volatiles from cotton. Environ Entomol. 2010; 39(2): 600–609. PubMed Abstract | Publisher Full Text
10. Dweck HK, Svensson GP, Gündüz EA, et al.: Kairomonal response of the parasitoid, Bracon hebetor Say, to the male-produced sex pheromone of its host, the greater waxmoth, Galleria mellonella (L.). J Chem Ecol. 2010; 36(2): 171–178. PubMed Abstract | Publisher Full Text
11. Beyaert I, Wäschke N, Scholz A, et al.: Relevance of resource-indicating key volatiles and habitat odour for insect orientation. Anim Behav. 2010; 79(5): 1077–1086. Publisher Full Text
12. Wajnberg É, Bernstein C, van Alphen J: Behavioral ecology of insect parasitoids: from theoretical approaches to field applications. Wiley-Blackwell, Malden, MA, 2008. Publisher Full Text
13. Najar-Rodriguez AJ, Friedli M, Klaiber J, et al.: Aphid-deprivation from Brassica plants results in increased isothiocyanate release and parasitoid attraction. Chemoecology. 2015; 25(6): 303–311. Publisher Full Text
14. van Wijk M, de Bruijn PJ, Sabelis MW: Complex odor from plants under attack: herbivore’s enemies react to the whole, not its parts. PLoS One. 2011; 6(7): e21742. PubMed Abstract | Publisher Full Text | Free Full Text
15. Mumm R, Hilker M: The significance of background odour for an egg parasitoid to detect plants with host eggs. Chem Senses. 2005; 30(4): 337–343. PubMed Abstract | Publisher Full Text
16. Tamiru A, Bruce T, Woodcock C, et al.: Chemical cues modulating electrophysiological and behavioural responses in the parasitic wasp Cotesia sesamiae. Can J Zool. 2015; 93(4): 281–287. Publisher Full Text
17. Morawo T, Burrows M, Fadamiro H: Dataset 1 in: Electroantennogram response of the parasitoid, Microplitis croceipes to host-related odors: The discrepancy between relative abundance and level of antennal responses to volatile compound. F1000research. 2016. Data Source

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¹ Department of Entomology & Plant Pathology, Auburn University, Auburn, USA
² Division of Parasitic Diseases and Malaria- Entomology, Centers for Disease Control and Prevention, Atlanta, USA

Competing interests

No competing interests were disclosed.

Grant information

The author(s) declared that no grants were involved in supporting this work.

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© 2017 Morawo T et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Data associated with the article are available under the terms of the Creative Commons Zero "No rights reserved" data waiver (CC0 1.0 Public domain dedication).

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Morawo T, Burrows M and Fadamiro H. Electroantennogram response of the parasitoid, Microplitis croceipes to host-related odors: The discrepancy between relative abundance and level of antennal responses to volatile compound [version 2; peer review: 4 approved]. F1000Research 2017, 5:2725 (https://doi.org/10.12688/f1000research.10104.2)

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Torsten Meiners, Federal Research Centre for Cultivated Plants Ecological Chemistry, Plant Analysis and Stored Product Protection, Julius Kühn-Institut (JKI), Berlin, Germany

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General comments

This study investigated the EAG response of a parasitoid Microplitis croceipes to the volatiles emitted from its host, the cotton plant-fed Heliothis virescens larvae. 15 compounds were tested at the dose of 1 μg on the female ... Continue reading

General comments

This study investigated the EAG response of a parasitoid Microplitis croceipes to the volatiles emitted from its host, the cotton plant-fed Heliothis virescens larvae. 15 compounds were tested at the dose of 1 μg on the female antennae of M. croceipes. Different level of bioactivity of M. croceipes to these compounds were presented and discrepancy was observed between the relative abundance and level of antennal responses in parasitoids. In the end, the authors suggested that ecological relevance but not the relative abundance of these compounds weighted more on the EAG responses of M. croceipes. However, since there is no behavior bioassay showing that these host-released compounds were truly importantly in the host-seeking process, it is hard to tell the ecological relevance of those compounds (like decanal) with strong EAG responses. A more cautious conclusion would be appropriate.

Specific comments

Introduction: Please give more information about why the authors specifically stated that the Heliothis virescens larvae were cotten-fed in the lab. Will different food sources affect the compounds released from the insect bodies?

Method: Please justify why mass concentration was used in preparing the compounds. Different chemicals possess various molecular weight and vapor pressure. Therefore, the number of molecules delivered onto the antenna may be dramatically different. In addition, only female wasps were used in the experiments. Apparently females need to find host to lay eggs. Just curious to know what the male's EAG responses to these compounds or if there are any related studies.

Results: Since 50% of the EAG responses from blend volatiles were used as a standard to make comparison, it would be better to add the EAG response to the blend volatiles in the bar figure. In addition, please specify the EAG response to the control solvent (hexane).

Discussion: The authors initiated a good start to discuss some compounds in the blend may function as background odors to enhance olfactory contract. There are many excellent reviews about the possible mechanisms behind this pheromone, such as Riffell and Hildebrand (2016).The authors may discuss a little bit about the mechanisms.

Competing Interests: No competing interests were disclosed.

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Reviewer Report 10 Feb 2017

Torsten Meiners, Federal Research Centre for Cultivated Plants Ecological Chemistry, Plant Analysis and Stored Product Protection, Julius Kühn-Institut (JKI), Berlin, Germany

Approved with Reservations

https://doi.org/10.5256/f1000research.10885.r19230

The research note of Tolulope et al. reports EAG responses of the parasitic wasp Microplitis croceipes and relates the antennal responses to the relative abundance of the compounds in the odour bouquet of the larvae.

When looking ... Continue reading

The research note of Tolulope et al. reports EAG responses of the parasitic wasp Microplitis croceipes and relates the antennal responses to the relative abundance of the compounds in the odour bouquet of the larvae.

When looking at the relative abundance of a compound you might need to consider all environmentally occurring contexts and compounds. Microplitis is orientating to the host habitat first, then it locates the host plant in the habitat, and then the host. That means that plant odours play an important role (see Li et al.¹) and not only larval odours. In my opinion you have to rank the importance of odours according to all environmental contexts and consider the abundance of compounds in cotton or also in other relevant host (and habitat) plants. Heliothis feeds on more than 100 plant species, thus M. croceipes is confronted with the odour of this plants and with the odour of larvae having fed on these plants. Li et al.¹ have performed antennal studies with M. croceipes and cotton plant compounds and found similar responses to similar compounds as in your study. Heptanal was the most stimulating tested compound while caryophyllene was less stimulating. The the discrepancy you indicate in the title might be easily explained when including habitat and host plant volatiles.

The wasps in your study had the experience of living and hatching from larvae having fed on cotton. Thus they might have experience with the compounds you present in Table 1. It has been shown that M. croceipes can learn almost any compund (e.g. Olson et al.²).

In your discussion you point out that it might be the ecological relevance of a compound that determines the antennal response – however, Park et al.³ showed in electroantennogram studies that the antenna of M. croceipes is also responding to anthropogenic compounds with high sensitivity. Thus, the antennal response might not reflect the ecological relevance. This might be more reflected in the behavioural response, as you indicate in your discussion. And this might be fine-tuned by leaning in case of a parasitoid with a polyphagous host.

Minor points:

Methods: Why is 1 µg an optimal dose?

Data analyses: Differences …were analysed

References

1. Li Y, Dickens JC, Steiner WW: Antennal olfactory responsiveness ofMicroplitis croceipes (Hymenoptera: Braconidae) to cotton plant volatiles.J Chem Ecol. 1992; 18 (10): 1761-73 PubMed Abstract | Publisher Full Text
2. Olson DM, Rains GC, Meiners T, Takasu K, et al.: Parasitic wasps learn and report diverse chemicals with unique conditionable behaviors.Chem Senses. 2003; 28 (6): 545-9 PubMed Abstract
3. Park K, Zhu J, Harris J, Ochieng S, et al.: Electroantennogram responses of a parasitic wasp, Microplitis croceipes, to host-related volatile and anthropogenic compounds. Physiological Entomology. 2008; 26 (1): 69-77 Publisher Full Text

Competing Interests: No competing interests were disclosed.

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however I have significant reservations, as outlined above.

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Reviewer Report 06 Feb 2017

Yonggen Lou, National Key Laboratory of Rice Biology, Institute of Insect Science, Zhejiang University, Hangzhou, China

Approved

https://doi.org/10.5256/f1000research.10885.r19925

The manuscript reported the the relationship between the relative abundance of volatile chemical emitted from Heliothis virescens larvae and the antennal response by the larval parasitoid of the herbivore, Microplitis croceipes. By electroantennogram bioassays, the authors found that the level ... Continue reading

The manuscript reported the the relationship between the relative abundance of volatile chemical emitted from Heliothis virescens larvae and the antennal response by the larval parasitoid of the herbivore, Microplitis croceipes. By electroantennogram bioassays, the authors found that the level of parasitoid’s EAG response is not related to relative abundance of the volatile components in the blend. Since a chemical that elicits an EAG response in an insect does not mean to elicit a behavioral response, and a chemical eliciting a bigger EAG response does not mean to elicit a stronger behavioral response, these experiments seem little and the novelty and significance of this study seem limited.

Introduction: In a previous study, the authors have investigated the attractiveness of these individual volatile compounds to the parasitoid, thus it would be better to introduce these results briefly in the section of Introduction.

Methods: It has been well documented that an insect has different responsive ranges to different chemicals. Thus, only using one concentration of chemicals is not enough.

Discussion: Based on the previous results reported by the authors¹, 8 chemicals in the blend, including decanal and (E)-β-Caryophyllene, had a role in attraction of the parasitoid. The authors should give a discussion based on above results.

References

1. Morawo T, Fadamiro H: Identification of Key Plant-Associated Volatiles Emitted by Heliothis virescens Larvae that Attract the Parasitoid, Microplitis croceipes: Implications for Parasitoid Perception of Odor Blends.J Chem Ecol. 2016; 42 (11): 1112-1121 PubMed Abstract | Publisher Full Text

Competing Interests: No competing interests were disclosed.

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard.

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Reviewer Report 16 Jan 2017

Amanuel Tamiru, Max Planck Institute for Chemical Ecology (MPICE), Nairobi, Kenya

Approved

https://doi.org/10.5256/f1000research.10885.r19376

General comments:

This study examined the relationship between the relative abundance of a volatile organic compounds (VOCs) emitted by Heliothis virescens (Lepidoptera: Noctuidae) and level of antennal response by the larval parasitoid, Microplitis croceipes (Hymenoptera: Braconidae). The ... Continue reading

General comments:

This study examined the relationship between the relative abundance of a volatile organic compounds (VOCs) emitted by Heliothis virescens (Lepidoptera: Noctuidae) and level of antennal response by the larval parasitoid, Microplitis croceipes (Hymenoptera: Braconidae). The study builds on the previous work by Morawo & Fadamiro (2016) which identified key plant-associated volatiles emitted by cotton-fed H. virescens larvae that attract the parasitoid, M. croceipes. Here, the synthetic versions of 15 previously identified plant-associated volatiles emitted by H. virescens larvae were tested in electroantennogram (EAG) bioassays. The authors conclude that the level of parasitoid’s antennal response is not directly related to relative abundance of the volatile components rather influenced by the ecological relevance or functional role of the compound in the blend. It should be noted that identifying volatile compounds that insects detect through EAG is an initial step in understanding olfactory stimuli responsible for modulating insect behavior. Hence, behavioral studies with the identified EAG active compounds should be carried out, individually and as blends, to determine responses of parasitoids to the volatile compounds and explore their ecological or functional role. Though the authors intended to examine relationship between relative abundance of the VOCs and level of antennal responses, different levels of the volatile compounds used in the study and their corresponding EAG response is not shown. Rather, only one dose (1 µg) is used for all volatile compounds tested. The study would have been very informative if different levels of the test compounds are tested and their corresponding EAG response recorded.

Specific comments

Title: The title is appropriate for the content of the article; however, it can be made more concise. E.g. the first part of the existing title would adequate, i.e. ‘Electroantennogram response of the parasitoid, Microplitis croceipes to host-related odors’.

Introduction: The introduction clearly states the objective of the study. However, adequate background is missing in the area of herbivore emitted plant associated VOCs. Are these plant derived volatile compounds emitted by herbivore itself (after feeding) or are they adsorbed into the hervivore body during feeding process (e.g. from frass)

Methods and materials: The authors followed standard insect rearing (Lewis & Burton, 1970) and electroantennogram recording (Ngumbi et al., 2010) and data analysis procedures. However, the number of insect replicates used in the study is not clear. Was a single insect antennal preparation used to record EAG responses to the 15 compounds and control (hexane)? Was the abundance of volatile components varied based on the corresponding quantities in the natural headspace samples? The latter has not been specified in the methodology except mentioning ‘Test compounds were formulated in hexane at 0.1 μg/μl and delivered onto Whatman®No.1 filter paper strips at an optimum dose of 1 µg’.

Results: The results show that female M. croceipes showed varying EAG responses to test compounds. Notably, decanal which constituted only 1% of total blend emitted by cotton-fed H. virescens elicited the highest EAG response (0.82 mV); while (E)-β-caryophyllene, the most abundant component (29.2% of total blend), elicited a relatively low EAG response (0.17 mV) in the parasitoid antenna. This is possible as earlier reports also indicated compounds with highest EAG response may not necessarily be those emitted in largest quantity (Tamiru et al. 2015¹). Given the fact that the main research question of this study is examine the relationship between relative abundance and level of antennal responses, it would have been more informative to test different concentrations/amounts of the test compounds and their corresponding EAG response to reliably measure statistical significance of correlations between relative abundance of the compounds and level of EAG response.

Discussion: The authors discuss about the ecological relevance of a compounds. However, electrophysiological responses do not necessarily mean that a behavioral response will occur; rather it elucidates potential behaviorally relevant compounds. To fully explore the significance of the results, bioassays need to be carried out with identified compounds, both individually and as a blend, to determine the kind of behavioral response the volatile compounds trigger in the parasitoid and their ecological/functional role. I suggested authors to refer and perhaps include in their discussion the work by Tamiru et al. (2015)¹ which demonstrated combined use of electrophysiological and behavioral studies for better understanding of odor mediated behavior in insects.

References

1. Tamiru A, Bruce T, Woodcock C, Birkett M, et al.: Chemical cues modulating electrophysiological and behavioural responses in the parasitic waspCotesia sesamiae. Canadian Journal of Zoology. 2015; 93 (4): 281-287 Publisher Full Text

Competing Interests: No competing interests were disclosed.

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Amanuel Tamiru, Max Planck Institute for Chemical Ecology (MPICE), Nairobi, Kenya
Yonggen Lou, Zhejiang University, Hangzhou, China
Torsten Meiners, Julius Kühn-Institut (JKI), Berlin, Germany
Feng Liu, Michigan State University, East Lansing, USA

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11 Apr 2017 | for Version 2

Torsten Meiners, Federal Research Centre for Cultivated Plants Ecological Chemistry, Plant Analysis and Stored Product Protection, Julius Kühn-Institut (JKI), Berlin, Germany

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The authors provided more information on a previous study and on the methods in the revision. They furthermore introduced the research topic and discussed their results more comprehensively.

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Feng Liu, Department of Entomology, Michigan State University, East Lansing, MI, USA

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General comments

This study investigated the EAG response of a parasitoid Microplitis croceipes to the volatiles emitted from its host, the cotton plant-fed Heliothis virescens larvae. 15 compounds were tested at the dose of 1 μg on the female antennae of M. croceipes. Different level of bioactivity of M. croceipes to these compounds were presented and discrepancy was observed between the relative abundance and level of antennal responses in parasitoids. In the end, the authors suggested that ecological relevance but not the relative abundance of these compounds weighted more on the EAG responses of M. croceipes. However, since there is no behavior bioassay showing that these host-released compounds were truly importantly in the host-seeking process, it is hard to tell the ecological relevance of those compounds (like decanal) with strong EAG responses. A more cautious conclusion would be appropriate.

Specific comments

Introduction: Please give more information about why the authors specifically stated that the Heliothis virescens larvae were cotten-fed in the lab. Will different food sources affect the compounds released from the insect bodies?

Method: Please justify why mass concentration was used in preparing the compounds. Different chemicals possess various molecular weight and vapor pressure. Therefore, the number of molecules delivered onto the antenna may be dramatically different. In addition, only female wasps were used in the experiments. Apparently females need to find host to lay eggs. Just curious to know what the male's EAG responses to these compounds or if there are any related studies.

Results: Since 50% of the EAG responses from blend volatiles were used as a standard to make comparison, it would be better to add the EAG response to the blend volatiles in the bar figure. In addition, please specify the EAG response to the control solvent (hexane).

Discussion: The authors initiated a good start to discuss some compounds in the blend may function as background odors to enhance olfactory contract. There are many excellent reviews about the possible mechanisms behind this pheromone, such as Riffell and Hildebrand (2016).The authors may discuss a little bit about the mechanisms.

Competing Interests

No competing interests were disclosed.

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard.

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16 Views

10 Feb 2017 | for Version 1

Torsten Meiners, Federal Research Centre for Cultivated Plants Ecological Chemistry, Plant Analysis and Stored Product Protection, Julius Kühn-Institut (JKI), Berlin, Germany

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Approved With Reservations

The research note of Tolulope et al. reports EAG responses of the parasitic wasp Microplitis croceipes and relates the antennal responses to the relative abundance of the compounds in the odour bouquet of the larvae.

When looking at the relative abundance of a compound you might need to consider all environmentally occurring contexts and compounds. Microplitis is orientating to the host habitat first, then it locates the host plant in the habitat, and then the host. That means that plant odours play an important role (see Li et al.¹) and not only larval odours. In my opinion you have to rank the importance of odours according to all environmental contexts and consider the abundance of compounds in cotton or also in other relevant host (and habitat) plants. Heliothis feeds on more than 100 plant species, thus M. croceipes is confronted with the odour of this plants and with the odour of larvae having fed on these plants. Li et al.¹ have performed antennal studies with M. croceipes and cotton plant compounds and found similar responses to similar compounds as in your study. Heptanal was the most stimulating tested compound while caryophyllene was less stimulating. The the discrepancy you indicate in the title might be easily explained when including habitat and host plant volatiles.

The wasps in your study had the experience of living and hatching from larvae having fed on cotton. Thus they might have experience with the compounds you present in Table 1. It has been shown that M. croceipes can learn almost any compund (e.g. Olson et al.²).

In your discussion you point out that it might be the ecological relevance of a compound that determines the antennal response – however, Park et al.³ showed in electroantennogram studies that the antenna of M. croceipes is also responding to anthropogenic compounds with high sensitivity. Thus, the antennal response might not reflect the ecological relevance. This might be more reflected in the behavioural response, as you indicate in your discussion. And this might be fine-tuned by leaning in case of a parasitoid with a polyphagous host.

Minor points:

Methods: Why is 1 µg an optimal dose?

Data analyses: Differences …were analysed

References

1. Li Y, Dickens JC, Steiner WW: Antennal olfactory responsiveness ofMicroplitis croceipes (Hymenoptera: Braconidae) to cotton plant volatiles.J Chem Ecol. 1992; 18 (10): 1761-73 PubMed Abstract | Publisher Full Text
2. Olson DM, Rains GC, Meiners T, Takasu K, et al.: Parasitic wasps learn and report diverse chemicals with unique conditionable behaviors.Chem Senses. 2003; 28 (6): 545-9 PubMed Abstract
3. Park K, Zhu J, Harris J, Ochieng S, et al.: Electroantennogram responses of a parasitic wasp, Microplitis croceipes, to host-related volatile and anthropogenic compounds. Physiological Entomology. 2008; 26 (1): 69-77 Publisher Full Text

Competing Interests

No competing interests were disclosed.

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however I have significant reservations, as outlined above.

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15 Views

06 Feb 2017 | for Version 1

Yonggen Lou, National Key Laboratory of Rice Biology, Institute of Insect Science, Zhejiang University, Hangzhou, China

15 Views Cite this report Responses(0)

Approved

The manuscript reported the the relationship between the relative abundance of volatile chemical emitted from Heliothis virescens larvae and the antennal response by the larval parasitoid of the herbivore, Microplitis croceipes. By electroantennogram bioassays, the authors found that the level of parasitoid’s EAG response is not related to relative abundance of the volatile components in the blend. Since a chemical that elicits an EAG response in an insect does not mean to elicit a behavioral response, and a chemical eliciting a bigger EAG response does not mean to elicit a stronger behavioral response, these experiments seem little and the novelty and significance of this study seem limited.

Introduction: In a previous study, the authors have investigated the attractiveness of these individual volatile compounds to the parasitoid, thus it would be better to introduce these results briefly in the section of Introduction.

Methods: It has been well documented that an insect has different responsive ranges to different chemicals. Thus, only using one concentration of chemicals is not enough.

Discussion: Based on the previous results reported by the authors¹, 8 chemicals in the blend, including decanal and (E)-β-Caryophyllene, had a role in attraction of the parasitoid. The authors should give a discussion based on above results.

References

1. Morawo T, Fadamiro H: Identification of Key Plant-Associated Volatiles Emitted by Heliothis virescens Larvae that Attract the Parasitoid, Microplitis croceipes: Implications for Parasitoid Perception of Odor Blends.J Chem Ecol. 2016; 42 (11): 1112-1121 PubMed Abstract | Publisher Full Text

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No competing interests were disclosed.

I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard.

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19 Views

16 Jan 2017 | for Version 1

Amanuel Tamiru, Max Planck Institute for Chemical Ecology (MPICE), Nairobi, Kenya

19 Views Cite this report Responses(0)

Approved

General comments:

This study examined the relationship between the relative abundance of a volatile organic compounds (VOCs) emitted by Heliothis virescens (Lepidoptera: Noctuidae) and level of antennal response by the larval parasitoid, Microplitis croceipes (Hymenoptera: Braconidae). The study builds on the previous work by Morawo & Fadamiro (2016) which identified key plant-associated volatiles emitted by cotton-fed H. virescens larvae that attract the parasitoid, M. croceipes. Here, the synthetic versions of 15 previously identified plant-associated volatiles emitted by H. virescens larvae were tested in electroantennogram (EAG) bioassays. The authors conclude that the level of parasitoid’s antennal response is not directly related to relative abundance of the volatile components rather influenced by the ecological relevance or functional role of the compound in the blend. It should be noted that identifying volatile compounds that insects detect through EAG is an initial step in understanding olfactory stimuli responsible for modulating insect behavior. Hence, behavioral studies with the identified EAG active compounds should be carried out, individually and as blends, to determine responses of parasitoids to the volatile compounds and explore their ecological or functional role. Though the authors intended to examine relationship between relative abundance of the VOCs and level of antennal responses, different levels of the volatile compounds used in the study and their corresponding EAG response is not shown. Rather, only one dose (1 µg) is used for all volatile compounds tested. The study would have been very informative if different levels of the test compounds are tested and their corresponding EAG response recorded.

Specific comments

Title: The title is appropriate for the content of the article; however, it can be made more concise. E.g. the first part of the existing title would adequate, i.e. ‘Electroantennogram response of the parasitoid, Microplitis croceipes to host-related odors’.

Introduction: The introduction clearly states the objective of the study. However, adequate background is missing in the area of herbivore emitted plant associated VOCs. Are these plant derived volatile compounds emitted by herbivore itself (after feeding) or are they adsorbed into the hervivore body during feeding process (e.g. from frass)

Methods and materials: The authors followed standard insect rearing (Lewis & Burton, 1970) and electroantennogram recording (Ngumbi et al., 2010) and data analysis procedures. However, the number of insect replicates used in the study is not clear. Was a single insect antennal preparation used to record EAG responses to the 15 compounds and control (hexane)? Was the abundance of volatile components varied based on the corresponding quantities in the natural headspace samples? The latter has not been specified in the methodology except mentioning ‘Test compounds were formulated in hexane at 0.1 μg/μl and delivered onto Whatman®No.1 filter paper strips at an optimum dose of 1 µg’.

Results: The results show that female M. croceipes showed varying EAG responses to test compounds. Notably, decanal which constituted only 1% of total blend emitted by cotton-fed H. virescens elicited the highest EAG response (0.82 mV); while (E)-β-caryophyllene, the most abundant component (29.2% of total blend), elicited a relatively low EAG response (0.17 mV) in the parasitoid antenna. This is possible as earlier reports also indicated compounds with highest EAG response may not necessarily be those emitted in largest quantity (Tamiru et al. 2015¹). Given the fact that the main research question of this study is examine the relationship between relative abundance and level of antennal responses, it would have been more informative to test different concentrations/amounts of the test compounds and their corresponding EAG response to reliably measure statistical significance of correlations between relative abundance of the compounds and level of EAG response.

Discussion: The authors discuss about the ecological relevance of a compounds. However, electrophysiological responses do not necessarily mean that a behavioral response will occur; rather it elucidates potential behaviorally relevant compounds. To fully explore the significance of the results, bioassays need to be carried out with identified compounds, both individually and as a blend, to determine the kind of behavioral response the volatile compounds trigger in the parasitoid and their ecological/functional role. I suggested authors to refer and perhaps include in their discussion the work by Tamiru et al. (2015)¹ which demonstrated combined use of electrophysiological and behavioral studies for better understanding of odor mediated behavior in insects.

References

1. Tamiru A, Bruce T, Woodcock C, Birkett M, et al.: Chemical cues modulating electrophysiological and behavioural responses in the parasitic waspCotesia sesamiae. Canadian Journal of Zoology. 2015; 93 (4): 281-287 Publisher Full Text

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[1] 1. De Moraes CM, Lewis WJ, Paré PW, et al.: Herbivore-infested plants selectively attract parasitoids. Nature. 1998; 393: 570–573. Publisher Full Text

[2] 2. Turlings TC, Wäckers F: Recruitment of predators and parasitoids by herbivore-injured plants. Adv Insect Chem Ecol. 2004; 2: 21–75. Reference Source

[3] 3. de Rijk M, Krijn M, Jenniskens W, et al.: Flexible parasitoid behaviour overcomes constraint resulting from position of host and nonhost herbivores. Anim Behav. 2016; 113: 125–135. Publisher Full Text

[4] 4. Elzen GW, Williams HJ, Vinson SB: Role of diet in host selection of Heliothis virescens by parasitoid Campoletis sonorensis (Hymenoptera: Ichneumonidae). J Chem Ecol. 1984; 10: 1535–1541. Publisher Full Text

[5] 5. Morawo T, Fadamiro H: Identification of key plant-associated volatiles emitted by Heliothis virescens larvae that attract the parasitoid, Microplitis croceipes: implications for parasitoid perception of odor blends. J Chem Ecol. 2016; 1–10. PubMed Abstract | Publisher Full Text

[6] 6. Clavijo McCormick A, Gershenzon J, Unsicker SB: Little peaks with big effects: establishing the role of minor plant volatiles in plant-insect interactions. Plant Cell Environ. 2014; 37(8): 1836–1844. PubMed Abstract | Publisher Full Text

[7] 7. Lewis WJ, Burton RL: Rearing Microplitis croceipes in the laboratory with Heliothis zea as host. J Econ Entomol. 1970; 63(2): 656–658. Publisher Full Text

[8] 8. Ngumbi E, Chen L, Fadamiro H: Electroantennogram (EAG) responses of Microplitis croceipes and Cotesia marginiventris and their lepidopteran hosts to a wide array of odor stimuli: correlation between EAG response and degree of host specificity? J Insect Physiol. 2010; 56(9): 1260–1268. PubMed Abstract | Publisher Full Text

[9] 9. Yu H, Zhang Y, Wyckhuys KA, et al.: Electrophysiological and behavioral responses of Microplitis mediator (Hymenoptera: Braconidae) to caterpillar-induced volatiles from cotton. Environ Entomol. 2010; 39(2): 600–609. PubMed Abstract | Publisher Full Text

[10] 10. Dweck HK, Svensson GP, Gündüz EA, et al.: Kairomonal response of the parasitoid, Bracon hebetor Say, to the male-produced sex pheromone of its host, the greater waxmoth, Galleria mellonella (L.). J Chem Ecol. 2010; 36(2): 171–178. PubMed Abstract | Publisher Full Text

[11] 11. Beyaert I, Wäschke N, Scholz A, et al.: Relevance of resource-indicating key volatiles and habitat odour for insect orientation. Anim Behav. 2010; 79(5): 1077–1086. Publisher Full Text

[12] 12. Wajnberg É, Bernstein C, van Alphen J: Behavioral ecology of insect parasitoids: from theoretical approaches to field applications. Wiley-Blackwell, Malden, MA, 2008. Publisher Full Text

[13] 13. Najar-Rodriguez AJ, Friedli M, Klaiber J, et al.: Aphid-deprivation from Brassica plants results in increased isothiocyanate release and parasitoid attraction. Chemoecology. 2015; 25(6): 303–311. Publisher Full Text

[14] 14. van Wijk M, de Bruijn PJ, Sabelis MW: Complex odor from plants under attack: herbivore’s enemies react to the whole, not its parts. PLoS One. 2011; 6(7): e21742. PubMed Abstract | Publisher Full Text | Free Full Text

[15] 15. Mumm R, Hilker M: The significance of background odour for an egg parasitoid to detect plants with host eggs. Chem Senses. 2005; 30(4): 337–343. PubMed Abstract | Publisher Full Text

[16] 16. Tamiru A, Bruce T, Woodcock C, et al.: Chemical cues modulating electrophysiological and behavioural responses in the parasitic wasp Cotesia sesamiae. Can J Zool. 2015; 93(4): 281–287. Publisher Full Text

[17] 17. Morawo T, Burrows M, Fadamiro H: Dataset 1 in: Electroantennogram response of the parasitoid, Microplitis croceipes to host-related odors: The discrepancy between relative abundance and level of antennal responses to volatile compound. F1000research. 2016. Data Source

Electroantennogram response of the parasitoid, Microplitis croceipes to host-related odors: The discrepancy between relative abundance and level of antennal responses to volatile compound

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Revised Amendments from Version 1

Introduction

Table 1. Composition of headspace volatile organic compounds emitted by cotton-fed Heliothis virescens larvae.

Methods and materials

Insects

EAG recording

Data analyses

Results

Figure 1. EAG responses of Microplitis croceipes to synthetic compounds.

Discussion

Data availability

Author contributions

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