Dispersal Capacity of Trichogramma for the Management of Duponchelia fovealis

Round 1

Reviewer 1 Report

Comments and Suggestions for Authors

The paper provides information on the dispersion capacity of a parasitoid used for the biological control af an important pest of strawberries, the invasive Duponchelia fovealis.

 The paper is quite well written although there some issues to be fixed to guarantee better clarity and readability.

Please check the attached file for minor corrections. Specific comments are below.

 

Title

 fovealis: F should not be in capital letter

 

Abstract

L17-18 The context should be specified: D. fovealis is an invasive pest of strawberries in Brazil.

L22-23 in this case there are too many unnecessary details on the location

L27-28 sentence non clear, please rephrase

 

Introduction

L37-38 this sentence is too generic, please be more specific

L39-42 some more details on the pest (its origin, how it was introduced etc) as well as on the stage causing damage and the type of damage would be useful, together with naming what are the current management methods for this pest

L48 since no single species is named, the subject are parasitoids, therefore it should be “these parasitoids”

L50 “parasitization of a large number of lepidopteran species” per se is not a favourable argument unless the target lepidopterans are all pest species. The threat to non target Lepidoptera biodiversity might in fact be an issue

L50-61 this part is too generic, there must be a paragraph on the chosen parasitoid: why was T. pretiosum chosen? What about its biology?

 

Materials and methods

L97 a dot is missing after D

L106 please give more details on the tunnels: were them totally closed on all sides, from top to bottom?  What were the conditions inside (temperature/humidity)? Did you have any datalogger for these parameters? How many tunnels in total were used for the trial?

L128-129 please cite explicitly which where the treatments and the number of replicates for each treatment. This sentence is not clear: what does “these” refer to?

 

Results

Table 1 Please explain the meaning of all the acronyms in the table.

Table 3 Please explain the meaning of EPM and CV

 

References

Please check that ALL scientific names are in italics

Comments for author File: Comments.pdf

Comments on the Quality of English Language

Some scientific terms should be revised as suggested

Author Response

First of all, we would like to thank you for taking the time to read and for the suggestions you made to our manuscript. All suggestions were accepted and corrected in the original manuscript. The changes are highlighted in yellow.

 

Comments 1: Title -  fovealis: F should not be in capital letter

Response 1: the specific epithet was changed to lowercase.

 

Comments 2: Abstract - L17-18 The context should be specified: D. fovealis is an invasive pest of strawberries in Brazil.

Response 2: Rewritten: "The European pepper moth (Duponchelia fovealis) is predominant in the main strawberry production areas, including Brazil, as an important invasive pest and causes substantial damage to the crop."

 

Comments 3: L22-23 in this case there are too many unnecessary details on the location

Response 3: Rewrited to "The experiments were carried out on strawberry farms in the mountainous region of Espírito Santo."

 

Comments 4: L27-28 sentence non clear, please rephrase

Response 4: Reformulated to "After the initial 24 hours, new eggs were placed to replace the infested ones; the replacement was repeated at 48 and 72 hours."

 

Comments 5: L37-38 this sentence is too generic, please be more specific

Response 5: Reformulated to "Strawberry production is of great social and economic importance in Brazil. However, the crop is highly sensitive and frequently attacked by harmful agents, such as pests and diseases [1,2,3]."

 

Comments 6: L39-42 some more details on the pest (its origin, how it was introduced etc) as well as on the stage causing damage and the type of damage would be useful, together with naming what are the current management methods for this pest

Response 6: Reformulated to "The European pepper moth, Duponchelia fovealis Zeller, 1847 (Lepidoptera: Crambidae), is a polyphagous insect that was introduced into Brazil in 2007, quickly established itself, and is now widespread in the country's main strawberry production fields. Adults of D. fovealis lay eggs on the abaxial surface of the plant's low-lying leaves close to the ground. After hatching, the caterpillars, from neonates to final instars, feed on the leaves, causing significant damage to strawberry crops, mainly due to the lack of efficient management methods [1,2,4,5]."

 

Comments 7: L48 since no single species is named, the subjects are parasitoids, therefore it should be "these parasitoids"

Response 7: The subject was corrected.

 

Comments 8: L50 "parasitization of a large number of lepidopteran species" per se is not a favourable argument unless the target lepidopterans are all pest species. The threat to non target Lepidoptera biodiversity might in fact be an issue

Response 8: Reformulated to "This parasitoid species is widely known as an alternative for controlling pests of agricultural importance, being reported parasitizing eggs of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) [10], Heraclides astyalus (Godart, 1819) (Lepidoptera: Papilionidae) in Citrus sp. [11] and has high potential for use in D. fovealis. Arguments in favor of using these parasitoids include their ease of rearing in alternative hosts at a lower cost than natural hosts, wide geographic distribution, specialization, and efficiency in parasitizing [11,12,13]. "

 

Comments 9: L50-61 this part is too generic, there must be a paragraph on the chosen parasitoid: why was T. pretiosum chosen? What about its biology?

Response 9: Reformulated to "The origin of the species T. pretiosum is unknown, but it is naturally recurrent in the Americas and is the most commercialized species in Brazil for inundative release. The distribution of this species is recorded in 10 of the 12 countries of South America, and, in Brazil, it is found naturally in 15 of the 26 Brazilian states [9]. "

 

Comments 10: Materials and methods - L97 a dot is missing after D

 Response 10: The correction was made. "2.1. Evaluation of the dispersal of T. pretiosum in strawberry plants under low tunnel cultivation for parasitism of D. fovealis eggs"

 

Response 11: L106 please give more details on the tunnels: were them totally closed on all sides, from top to bottom? What were the conditions inside (temperature/humidity)? Did you have any datalogger for these parameters? How many tunnels in total were used for the trial?

Comments 11: Rewritten to "The experiment was installed under field conditions, that is, the climatic and management conditions were those typically found in the agricultural operation in question, with no additional control or monitoring of environmental conditions.

Four strawberry tunnels measuring ~1.20 m wide and 50 m long were selected. The low tunnel was built following the recommendations of Santos and Medeiros [19]. The structure was made with galvanized wire No. 6 arches at a minimum height of 80 cm, and the spacing between the arches was between 1.20 and 1.50 m. The structure was covered entirely with nonwoven fabrics (TNT). "

 

Comments 12: L128-129 please cite explicitly which where the treatments and the number of replicates for each treatment. This sentence is not clear: what does "these" refer to?

Response 12: Rewritten "A randomized block design with 4 tunnels was used. Each tunnel was considered a block, and the blocks were selected at a distance of >15 m between them. "

 

Response 13: Results - Table 1 Please explain the meaning of all the acronyms in the table.

Comments 13: Explanation: "¹ FV: Source of variation; ² Df: degree of freedom; ³ SQ: sum of squares; ⁴ QM: mean squares; ⁵ Fc: Observed F value; ⁶ P>F: F value in relation to the observed p-value; ⁷CV: coefficient of variation. *Significant values at the 5% significance level."

 

Response 14: Table 3 Please explain the meaning of EPM and CV

Comments 14: EPM stands for standard error term, however during an error during translation. The error has been corrected. "Mean values (± standard error) " "² CV: coefficient of variation."

 

Comments 15:  References

Please check that ALL scientific names are in italics

Response 15: All the scientific names were checked.

Author Response File: Author Response.pdf

Reviewer 2 Report

Comments and Suggestions for Authors

General comments

The manuscript "Dispersion Capacity of Trichogramma for the Management of Duponchelia Fovealis" by Pratissoli et al. reports on the dispersal of Trichogramma pretiosum in a strawberry crop in a low tunnel system after parasitoid release. Dispersal of Trichogramma spp. under practical conditions is an interestic topic that has to be studied specifically for different crops, and this study provides a new case in a low tunnel system.   Title: the specific epithet Fovealis has to be written in small caps. I suggest dispersal instead of dispersion.
    
Introduction: report on the original geographical distribution of Trichogramma pretiosum, and examples for its previous use for biological control.   Material and methods:
Please describe how parasitism was evaluated (key words: black eggs, superparasitism, parasitoid-induced mortality)
What was the sex-ratio of the parasitoid? We are interested in the ratio of one Duponchelia fovealis egg for X female parasitoids (1:?) The valid name is Ephestia kuehniella, not Anagasta kuehniella.   Results
Explain the different colours in Figs 2 and 3   Discussion
4.1. Release times and parasitism
How to improve the activity of the parasitoids after 48 h? -provide honey and / or prepare the release units for staggered emergence 4.2. Estimation of dispersal ability
You state the strawberry plant was a physical barrier. What is your estimate for the surface area of a strawberry plant? With this data, you can compare with results previously obtained for other crops.
You cited results for tomato plants, the hairy surface of plants also hinder the dispersal of Trichogramma spp. How smooth was the surface of your strawberry plant?
Interestingly Quednau (1958) also found Trichogramma to walk 14 m in 24h.
Quednau, W. Über einige Orientierungsweisen des EiparasitenTrichogramma (Hym. Chalcididae) auf Grund von Licht- und Schwerereizen. Anzeiger für Schädlingskunde 31, 83–85 (1958). https://doi.org/10.1007/BF02290031

specific comments
old:
Table 1 Parasitism of Trichogramma pretiosum within 15 m of the release point,
new:
Table 1 Parasitism of Trichogramma pretiosum within 15 m from the release point,  

Comments on the Quality of English Language

Some scientific terms should be revised as suggested

Author Response

Comments 1: The manuscript "Dispersion Capacity of Trichogramma for the Management of Duponchelia Fovealis" by Pratissoli et al. reports on the dispersal of Trichogramma pretiosum in a strawberry crop in a low tunnel system after parasitoid release. Dispersal of Trichogramma spp. under practical conditions is an interesting topic that has to be studied specifically for different crops, and this study provides a new case in a low tunnel system.   Title: the specific epithet Fovealis has to be written in small caps. I suggest dispersal instead of dispersion.

Response 1: We changed the Title suggestions for " Dispersal Capacity of Trichogramma for the Management of Duponchelia fovealis"

 

Comments 2 : Introduction: report on the original geographical distribution of Trichogramma pretiosum, and examples for its previous use for biological control. 

Response 2: We have rewrite the paragraph to:

"Parasitoids of the genus Trichogramma Westwood (Hymenoptera: Trichogrammatidae) are natural enemies used with significant frequency in biological pest control and are distributed worldwide [4,5,6]. The species T. pretiosum is reported to parasitize lepidopteran eggs, mainly those of agricultural importance, such as eggs of Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae) [6], Heraclides astyalus (Godart, 1819) (Lepidoptera: Papilionidae) in Citrus sp. [7] and has a high potential for use in D. fovealis."

 

Comments 3: Material and methods:
Please describe how parasitism was evaluated (key words: black eggs, superparasitism, parasitoid-induced mortality)

Response 3: We rewrite the phrase to: "where they remained until parasitism was assessed by observing the darkening of the eggs and confirmed after the emergence of the individuals. (Figure 1C)."

 

Comments 4: What was the sex-ratio of the parasitoid? We are interested in the ratio of one Duponchelia fovealis egg for X female parasitoids (1:?) The valid name is Ephestia kuehniella, not Anagasta kuehniella.   

Response 4: We only use females for field release, so we do not mention the sexual ratio, however we have already corrected and described this information in the text. In the text, it was mentioned that the release ratio was 1:4, as recommended for the trichogramma species: "Parasitoids were released in the tunnel's center at the recommended ratio of 1:4 (egg/parasitoid) using cartons containing the parasitoid species.".  We have changed the name for Ephestia kuehniella.

Comments 5: Results
Explain the different colours in Figs 2 and 3   

Response 5: The continuous vertical lines represent the point of release of the parasitoids and the curves represented by solid lines correspond to the parasitism area covered by the releases. The different colors simulate only the main position of each tunnel and the estimated area of parasitism of T. pretiosum; for example, the continuous vertical line in green simulates a main tunnel, and the dashed lines the parasitism area of 14.21 linear m; the same applies to the other colors.

 

Comments 6: Discussion
4.1. Release times and parasitism
How to improve the activity of the parasitoids after 48 h? -provide honey and / or prepare the release units for staggered emergence 

Response 6: According to studies conducted by Pratissoli et al. (2019), biologically, the potential of the Trichogramma individual is more affected by temperatures and climatic factors than by food. The greatest potential for parasitism occurs in the first 24 hours of life. Therefore, the provision of honey or food could prolong the lifespan of individuals but would interfere very little with the parasitism capacity. Studies with staggered release could be carried out to prolong the parasitism activity, however, it was not carried out in this experiment.

 

Comments 7: 4.2. Estimation of dispersal ability
You state the strawberry plant was a physical barrier. What is your estimate for the surface area of a strawberry plant? With this data, you can compare with results previously obtained for other crops.
You cited results for tomato plants, the hairy surface of plants also hinder the dispersal of Trichogramma spp. How smooth was the surface of your strawberry plant?

Response 7: In this experiment, the leaf area was not evaluated; the hypothesis was formulated according to the plant architecture based on the methodology for evaluating the dispersion capacity of Trichogramma proposed by Pratissoli et al., 2019. In the case of the strawberry plant, the barrier is conditioned by the large number of leaves that the plant has.

 

Comments 8:specific comments
old: Table 1 Parasitism of Trichogramma pretiosum within 15 m of the release point,
new: Table 1 Parasitism of Trichogramma pretiosum within 15 m from the release point,  

Response 8: We have changed the title of the table for the suggested one.

Author Response File: Author Response.pdf

Reviewer 3 Report

Comments and Suggestions for Authors

Dear Authors, the manuscript “Dispersion capacity of Trichogramma for the management of Duponchelia fovealis” would be potentially useful in the application of the parasitoid Trichogramma pretiosum in biological control. However, considering the specific experimental conditions (1.2 m wide tunnel), it is my opinion that the evaluation of the dispersion capacity is not supported by a suitable methodology. In particular, the classic method of sentinel-eggs at different distances from the launch point was applied with increasing density of eggs (without justifying the reason). The decreasing parasitization with increasing distance (as expected) is influenced by the increase in available sentinel-eggs. I consider this methodological aspect fundamental, since it probably leads to the underestimation of the real dispersal capacity of the parasitoid. Consequently, further detailed reviews are of little importance.

Author Response

Comments 1:Dear Authors, the manuscript “Dispersion capacity of Trichogramma for the management of Duponchelia fovealis” would be potentially useful in the application of the parasitoid Trichogramma pretiosum in biological control. However, considering the specific experimental conditions (1.2 m wide tunnel), it is my opinion that the evaluation of the dispersion capacity is not supported by a suitable methodology. In particular, the classic method of sentinel-eggs at different distances from the launch point was applied with increasing density of eggs (without justifying the reason). The decreasing parasitization with increasing distance (as expected) is influenced by the increase in available sentinel-eggs. I consider this methodological aspect fundamental, since it probably leads to the underestimation of the real dispersal capacity of the parasitoid. Consequently, further detailed reviews are of little importance.

 

 

Respond: Dear reviewer, we appreciate your time reading and suggestions for improving this work. We based this research on the studies of Fournier and Boivin (2000) regarding dispersion and release time. We believe that the study can facilitate the release mechanism in our research region, bringing more accurate information to rural producers. Based on the reviewer's comments and other reviewers' suggestions, we have reworded the methodology. We hope that this will make the text easier to understand. Any changes made to the text have been highlighted in yellow.

Round 2

Reviewer 1 Report

Comments and Suggestions for Authors

The authors accurately replied to all the issues raised. Now the paper could be accepted.

Author Response

Dear reviewer,
We would like to thank you for taking the time to make suggestions for our article and also for accepting it.

Reviewer 2 Report

Comments and Suggestions for Authors

Several aspects have not been considered in the revised version.

The background to my suggestion to write about the released parasitoid T. pretiosum in the introduction and materials and methods: There is a long tradition to use natve species of Trichogramma for biological control to prevent negative effects of invasive species on the native fauna, e.g. in France, even geographical strains of Trichgramma-species have to be registered for biological control. Trichgramma-species are polyphagous egg parasitoids and a potential thread to endangered butterflies. COnsequently, the question is: What is the original natural distribution of T. pretiosum, is it native to Brazil, and where does the relaesed strain originated?

The aspect of the surface of the crop hasn't beed addressed as well. E.g. corn leafs are smooth, tomato leaves have sparse adherent hairs, and strawberry dense semi-erect hairs which create a much larger surface for the very small parasitoids to travel. Finally, parasitism is dependent on the surface to be searched and the number of females released. It should be checked if the results obtained here are in line with other studies, and if not why.

Finally, the number of females relased is still unknown (important for comparison with other studies, see above). The new sentence is:
"After artificial infestation, female individuals of T. pretiosum were released" - ok, but how many? This can be found out by checkíng the sex-ratio of the respective strain (this is strain-specific, not species-specific in T. pretiosum).

 

Author Response

First of all, we would like to thank you again for reading this article and for your suggestions for our manuscript. All of the suggestions were accepted and corrected in the original manuscript, which is highlighted in yellow.

 

Comments 1: The background to my suggestion to write about the released parasitoid T. pretiosum in the introduction and materials and methods: There is a long tradition to use native species of Trichogramma for biological control to prevent negative effects of invasive species on the native fauna, e.g. in France, even geographical strains of Trichgramma-species have to be registered for biological control. Trichgramma species are polyphagous egg parasitoids and a potential threat to endangered butterflies. Consequently, the question is: What is the original natural distribution of T. pretiosum, is it native to Brazil, and where does the relaesed strain originated?

Response 1: We reformulated for "The origin of the species T. pretiosum is unknown, but it is naturally recurrent in the Americas and is the most commercialized species in Brazil for inundative release. The distribution of this species is recorded in 10 of the 12 countries of South America, and, in Brazil, it is found naturally in 15 of the 26 Brazilian states [9]."

 

Comments 2:The aspect of the surface of the crop hasn't beed addressed as well. E.g. corn leafs are smooth, tomato leaves have sparse adherent hairs, and strawberry dense semi-erect hairs which create a much larger surface for the very small parasitoids to travel. Finally, parasitism is dependent on the surface to be searched and the number of females released. It should be checked if the results obtained here are in line with other studies, and if not why.

Response 2: Thank you for the comment, we believe that the point discussed in the paragraph below, which belongs to the discussion topic, provides the answers to this question.

"In this case, the strawberry plant was a physical barrier to the dispersion of the parasitoid due to the plant's leaf density and the presence of trichomes on the leaves." 

"Control efficiency is directly related to the uniform distribution of the parasitoid [8,24]. Therefore, the results aimed to satisfy this condition. The calculated mean distance and the dispersal area provided greater homogeneity in the parasitoid's coverage of the area and, consequently, greater efficiency in controlling D. fovealis by T. pretiosum.

           The recommendation for parasitoid release may change depending on the crop type, planting density, and intensity of pest infestation in the field [8,24,28]. For fruit trees, they can vary from 70,000 to 3.8 million parasitoids per hectare [34,35]. For staked tomatoes, the recommendation is 576,000 Trichogramma released every eight days [36], while in Europe, the recommendation is 150,000 to 300,000 Trichogramma released every seven days in maize [37]."

"Based on the proposed estimates of the dispersal capacity of T. pretiosum for the control of D. fovealis, it is recommended that 93,000 female parasitoids be released at three-day intervals for each hectare of strawberry plants."

 

Comments 3:Finally, the number of females relased is still unknown (important for comparison with other studies, see above). The new sentence is:
"After artificial infestation, female individuals of T. pretiosum were released" - ok, but how many? This can be found out by checkíng the sex-ratio of the respective strain (this is strain-specific, not species-specific in T. pretiosum).

Response 3: We add the information in the following paragraph "The increasing number of eggs based on distance was to preserve the turgidity of the more distant eggs and avoid their unavailability due to parasitism. After artificial infestation, approximately 2400 female individuals of T. pretiosum were released early in the day, immediately after hatching and in the middle of the bed, in each tunnel according to its treatment. The average radius of action and the dispersion area of ​​the parasitoid were based on the methodology of Dobzhansky & Wright [20] with adaptations for the cultivation conditions found in Espírito Santo."

 

Author Response File: Author Response.pdf

Reviewer 3 Report

Comments and Suggestions for Authors

Dear Authors, I have carefully read the resubmitted manuscript “Dispersal capacity of Trichogramma for the management of Duponchelia fovealis” and your response to my observations. Contrary to your claims, the Materials and Methods section has not been rewritten. The article by Fournier and Boivin (2000) does not justify the increasing density of eggs used by you along the transect (indeed it is contrary to your methodology). Furthermore, Fournier and Boivin worked in an open field (with transects in 8 directions) and not in a tunnel (with transects in 2 mandatory directions). Furthermore, the reference article was never cited in the manuscript.

It is my opinion that the new version of the manuscript has not been improved.

Author Response

First of all, we would like to thank you again for reading this article and for your suggestions for our manuscript. We regret not meeting your expectations for improvements in the topics covered. This time, we worked hard to address the suggested points.

 

In this new version. We have improved the methodology by explaining the working conditions and describing the structure of the tunnels to make the method more reproducible.

E.g "

The experiment was installed under field conditions, that is, the climatic and management conditions were those typically found in the agricultural operation in question, with no additional control or monitoring of environmental conditions.

Four strawberry tunnels measuring ~1.20 m wide and 50 m long were selected. The low tunnel was built following the recommendations of Santos and Medeiros [19]. The structure was made with galvanized wire No. 6 arches at a minimum height of 80 cm, and the spacing between the arches was between 1.20 and 1.50 m. The structure was covered entirely with nonwoven fabrics (TNT). "

 

We also provided details about the initial infestation with the number of individuals used. Regarding the range of action and dispersion of the parasitoid, we provided the methodology on which our study was based.

"The increasing number of eggs based on distance was to preserve the turgidity of the more distant eggs and avoid their unavailability due to parasitism. After artificial infestation, approximately 2400 female individuals of T. pretiosum were released early in the day, immediately after hatching and in the middle of the bed, in each tunnel according to its treatment. The average radius of action and the dispersion area of ​​the parasitoid were based on the methodology of Dobzhansky & Wright [20] with adaptations for the cultivation conditions found in Espírito Santo."

 

We also better describe the description of the experimental design.

"A randomized block design with 4 tunnels was used. Each tunnel was considered a block, and the blocks were selected at a distance of >15 m between them. "

 

Considering also the latest suggestions about "the classical method of sentinel eggs at different distances from the release point was applied with increasing egg density (without justifying the reason)," we tried to answer this aspect in the methodology already described above: "The increasing number of eggs based on distance was to preserve the turgidity of the more distant eggs and avoid their unavailability due to parasitism." And so we believe that the discussion paragraph "The turgidity of the egg of D. fovealis may also have affected parasitism at greater distances. Eggs located at a greater distance from the parasitoid release point may lose their turgidity because they are more exposed to adverse environmental conditions, such as high temperature and low humidity, and when found by Trichogramma eggs, they are in a condition unsuitable for parasitism [30]." justifies the question.

 

The material from Fournier and Boivin (2000) was used only as a basis for our studies. Due to the differences (which you also noticed), we preferred not to cite it in the text. We read it and followed a direction for what was applicable in our region with the methodology used by the producers. We apologize if the way we wrote it gave the impression of something else. We did not want to give that impression.

 

In addition to the improvements described above, we have modified some aspects of the introduction and other points suggested by other reviewers. Thank you again for your time and availability. These are excellent points that you have made. We have done our best to explain the importance of the work based on your reviews.

Author Response File: Author Response.pdf

Round 3

Reviewer 3 Report

Comments and Suggestions for Authors

Dear Authors, I have read your explanations and the manuscript is sufficiently improved. However, I find it useful to provide some slight suggestions and corrections below.

Specific comments:

Line 88: please, delete “animal”;

Line 93: please, it is necessary to describe the diet used if it has been modified compared to the citation [19]; alternatively, delete “a modified version” if the diet used is the one reported in the citation [19];

Line 102: please, replace “A.” with “E.”;

Line 110-117: the sentence is too long. I suggest dividing the sentence, for better readability;

Line 126: please, delete “-“ after number;

Line 181: please, delete “1” in supersctipt;

Line 182: please, change “1” to superscript  before of  “Mean accumulated…”

Line 240: please, delete the sentence, since it is repeated later;

Line 279: please, write the “2” in superscript in "m2";

Line 340: please, replace “argumentative” with “augmentative”.

Author Response

Dear reviewer, thank you again for taking the time to read our work and for your suggestions. The requested changes have been made and are highlighted in the text.

 

Comments 1: Line 88: please, delete “animal”;

Response: deleted. "The adults were"

 

Comments 2: Line 93: please, it is necessary to describe the diet used if it has been modified compared to the citation [19]; alternatively, delete “a modified version” if the diet used is the one reported in the citation [19];

Response: Changed to "containing an artificial diet" only. 

 

Comments  3: Line 102: please, replace “A.” with “E.”;

Response: Replaced.

 

Comments 4: Line 110-117: the sentence is too long. I suggest dividing the sentence, for better readability;

Response: We divided the sentence for "To determine the displacement distance (dispersal ability) in linear meters and the number of release points within a low tunnel cultivated with strawberry plants, dispersal experiments were carried out on farms in the district of São João do Garrafão, municipality of Santa Maria de Jetibá, mountainous region of Espírito Santo (coordinates 1: 20°09'30'' S;40°59'05'' W; coordinates 2: 20°08'09'' S; 40°56'53'' W). Plants of the Albion cultivars were used, planted with a spacing of 0.3 m between rows and 0.3 m between plants in beds with three planting rows during the productive period (approximately four months after planting) in a low tunnel system, with one location per tunnel. "

 

Comments 5: Line 126: please, delete “-“ after number;

Response: The requested change has been made.

 

Comments 6: Line 181: please, delete “1” in supersctipt;

Response: The requested change has been made.

 

Comments  7: Line 182: please, change “1” to superscript  before of  “Mean accumulated…”

Response: The requested change has been made.

 

Comments 8: Line 240: please, delete the sentence, since it is repeated later;

Response : The requested change has been made.

 

Comments 9: Line 279: please, write the “2” in superscript in "m2";

Response: The requested change has been made.

 

Comments 10: Line 340: please, replace “argumentative” with “augmentative”.

Response: The requested change has been made.