Consideration of the Disease Complexes, the Missing Link to Correctly Analyze the Impact of Intercropping on Disease Development

Round 1

Reviewer 1 Report

Comments and Suggestions for Authors

The review addresses to an interesting disease control approach based on intercropping, which application has a number of beneficial effects in relation to the reduction of the pathogen spreading or the level of plant affection. For me, as a person working in the field of crop protection, this manuscript provided a lot of interesting information. It definitely deserves publication. I have only several rather minor remarks intended to improve it.

 

1) In general, it would be good to illustrate the positive effect of intercropping by some quantitative data. I found only one mentioning of a quantitative effect of intercropping (spore dispersal reduction) on page 9. However, I consider that authors could include more such data from the reviewed papers (reduction of various disease indices or even yield increase) in the text of the manuscript to provide a better understanding of the potential of such approach for agriculture.

2) Describing necrotrophic pathogens, it would be good to give a couple of examples (in the case of obligate pathogens, authors mention powdery mildew and rusts).

3) Page 11: “Crop diversification in annual systems can alter the microclimate and pathogen de-velopment in ways and with intensities that are difficult to predict.” - does it mean that in some cases such diversification is able to increase the disease development? I can suppose that some intercropping combinations may worsen the situation with the main crop not only in relation to the microclimate, but also for characteristics discussed in the previous sections of the manuscript. It would be interesting to know if there are any publications describing the “negative” intercropping attempts/variants, and the approximate ratio between such “positive” and “negative” publications, since such information (if any) would provide more proper evaluation of this approach and the prospects of its application.

 

Other minor comments are listed below.

 

Fig. 1: please, check for all phrases to be translated into English.

Page 6: Please, write a full name of the banana pathogen (C. fijiensis) as it is mentioned for the first time. The same is for other pathogens first mentioned in the further text.

Fig. 2: Chemical induction (not chimical). Please, correct.

Page 8: what are gelatinous plants? Please, give an explanation in the text.

Page 10: LAI: since this abbreviation first appears on the top of this page, it should be explained here, not at its second mentioning below at the same page.

Page 11, line 6: there are two “periods” words; please, remove one.

Fig. 3: what is LHT? This abbreviation is not explained in the figure capture. Also, check the text in Fig. 4 for misprints. Image quality is not good, small font is unreadable even at 600% magnification.

Line 13: “…very similar infection and host exploitation feeding strategies to exploit hosts...” - it seems that “host exploitation” and “to exploit hosts” phrases double each other. Please, check and correct, if necessary.

Comments on the Quality of English Language

English language is quite fine, though a minor eliting would improve the quality of the text.

Author Response

Comments and Suggestions for Authors

The review addresses to an interesting disease control approach based on intercropping, which application has a number of beneficial effects in relation to the reduction of the pathogen spreading or the level of plant affection. For me, as a person working in the field of crop protection, this manuscript provided a lot of interesting information. It definitely deserves publication. I have only several rather minor remarks intended to improve it.

 

• In general, it would be good to illustrate the positive effect of intercropping by some quantitative data. I found only one mentioning of a quantitative effect of intercropping (spore dispersal reduction) on page 9. However, I consider that authors could include more such data from the reviewed papers (reduction of various disease indices or even yield increase) in the text of the manuscript to provide a better understanding of the potential of such approach for agriculture.
• R: We agreed with this comment. We added in he text several examples indicating the impact of intercropping on the different mechanisms implicated in the development of epidemic.

2) Describing necrotrophic pathogens, it would be good to give a couple of examples (in the case of obligate pathogens, authors mention powdery mildew and rusts).

R: Correction done

3) Page 11: “Crop diversification in annual systems can alter the microclimate and pathogen development in ways and with intensities that are difficult to predict.” - does it mean that in some cases such diversification is able to increase the disease development? I can suppose that some intercropping combinations may worsen the situation with the main crop not only in relation to the microclimate, but also for characteristics discussed in the previous sections of the manuscript. It would be interesting to know if there are any publications describing the “negative” intercropping attempts/variants, and the approximate ratio between such “positive” and “negative” publications, since such information (if any) would provide more proper evaluation of this approach and the prospects of its application.

R: We have carried out a review of the literature on the impact of intercropping on the development of diseases. As a reminder, in this review we have chosen to focus on foliar diseases of fungal origin. After analysis, it appears that there are very few, if any, articles talking about the negative effect of intercropping on the epidemic development of this type of disease. Strangely, we found very few articles dealing with foliar diseases of fungal origin. Most articles dealing with fungal diseases focus mainly on soil-borne diseases. On the other hand, many articles deal with pest management. Only two main articles can underline a negative impact of intercropping on epidemic development of foliar disease, the review of Boudreau (2013), and the Metanalyses of Zhang et al (2019). In its review, Boudreau (2013) underlined that phenomenological research comparing disease in monocrops and intercrops, primarily due to foliar fungi, intercropping reduced disease in 73% of more than 200 studies. In their Metanalyses, Zhang et al (2019), the authors quantified the disease suppressive effect of intercropping cereals with legumes at different levels of N fertilizer. Authors showed that intercropping reduced disease incidence (measured by the odds ratio of disease occurrence) by 45% on average. This reduction was significant (P < 0.01) for four out of six studied pathogens: yellow rust (Puccinia striiformis f.sp. tritici) and mildew (Blumeria graminis) in wheat (Triticum aestivum), and chocolate spot (Botrytis fabae) and Fusarium wilt (Fusarium oxysporum) in faba bean (Vicia faba). Disease reduction was marginally significant for yellow rust in barley (Puccinia striiformis f.sp. hordei) (P < 0.10) and not significant for bean rust (Uromyces fabae). The reduction in disease incidence was greatest during the early stages of epidemics. N fertilizer strongly increased the incidence of powdery mildew of wheat, but it did not affect the incidence of the other diseases and it did not affect the effectiveness of intercropping as a management strategy for disease control.  

 

Other minor comments are listed below.

 

Fig. 1: please, check for all phrases to be translated into English.

R: Correction done

Page 6: Please, write a full name of the banana pathogen (C. fijiensis) as it is mentioned for the first time. The same is for other pathogens first mentioned in the further text.

R: Correction done

Fig. 2: Chemical induction (not chimical). Please, correct.

R: Correction done

Page 8: what are gelatinous plants? Please, give an explanation in the text.

R: We are sorry, it is a mistake. The word was removed, and a new sentence was added “, in the case of winter crops, the soil can be covered with freeze dried plants like the clover before the cash crop develops. Thus, by covering the soil in early autumn, the clover can prevent the auto-inoculum from spreading to the plants”

Page 10: LAI: since this abbreviation first appears on the top of this page, it should be explained here, not at its second mentioning below at the same page.

R: LAI means Leaf Area Index. The explanation was added in the text

Page 11, line 6: there are two “periods” words; please, remove one.

R: Correction done

Fig. 3: what is LHT? This abbreviation is not explained in the figure capture. Also, check the text in Fig. 4 for misprints. Image quality is not good, small font is unreadable even at 600% magnification.

R: Correction done

Line 13: “…very similar infection and host exploitation feeding strategies to exploit hosts...” - it seems that “host exploitation” and “to exploit hosts” phrases double each other. Please, check and correct, if necessary.

R: Correction done

Reviewer 2 Report

Comments and Suggestions for Authors

Comments and Suggestions for Authors

The manuscript titled “Consideration of the disease complexes, the missing link to correctly analyze the impact of intercropping on disease development” by Affichard et al. (Ref: Submission ID agronomy-2980008).

The manuscript is clear and presented in a well-structured manner. The cited references are current. However, I add some points here. he manuscript is clear and presented in a well-structured manner. However, it needs some minor revisions that would improve its quality. The required changes have been inserted into the manuscript. However, one of the most important modifications is the references, as the manuscript is severely lacking in scientific references.

 

Comments for author File: Comments.pdf

Author Response

Comments and Suggestions for Authors

The manuscript titled “Consideration of the disease complexes, the missing link to correctly analyze the impact of intercropping on disease development” by Affichard et al. (Ref: Submission ID agronomy-2980008).

The manuscript is clear and presented in a well-structured manner. The cited references are current. However, I add some points here. he manuscript is clear and presented in a well-structured manner. However, it needs some minor revisions that would improve its quality. The required changes have been inserted into the manuscript. However, one of the most important modifications is the references, as the manuscript is severely lacking in scientific references.

R: The review is based on scientific references (publications of research work), reviews and works presenting the ecological concepts to be used. It is true that for fungal leaf diseases, there are very few references and studies presenting the impact of crop associations on the development of this type of disease.

Reviewer 3 Report

Comments and Suggestions for Authors

The manuscript titled "Consideration of Disease Complexes: The Missing Link in Analyzing the Impact of Intercropping on Disease Development" exhibits commendable writing, comprehensiveness, and relevance to the field. However, to enhance its quality further, I have provided the following suggestions:

1.     Ensure uniformity in citation style throughout the manuscript. For instance, on the first page, citations like "a few species only [1]" and "synthetic inputs (Tilman 1999)" should follow a consistent format. Check the instruction for authors.

2.     Elaborate on the concept of "disease complexes" mentioned in the title by providing a definition or citing relevant literature. Additionally, clarify the term of "species complex" within the review.

3.     There is language not in English in Figure 1.

4.     Introduce species with their full scientific names upon first mention, such as C. musae, L. maculans, P. pinodella….

5.     The biggest problem I find in this article: Figure 2 should be closely linked to the corresponding content: The link between Fig 2 and 5.1, 5.2, 5.3, 5.4…is not tight; The direct/indirect effects are not clear; It is suggested that every point in Fig 2 should be connected well to the content.

6.     First appearance of abbreviation should include the full name of the term, such as LAI, IPM; check the entire article. And why LHT is only appear in the abstract?

Author Response

The manuscript titled "Consideration of Disease Complexes: The Missing Link in Analyzing the Impact of Intercropping on Disease Development" exhibits commendable writing, comprehensiveness, and relevance to the field. However, to enhance its quality further, I have provided the following suggestions:

Ensure uniformity in citation style throughout the manuscript. For instance, on the first page, citations like "a few species only [1]" and "synthetic inputs (Tilman 1999)" should follow a consistent format. Check the instruction for authors.

R: Correction done

Elaborate on the concept of "disease complexes" mentioned in the title by providing a definition or citing relevant literature. Additionally, clarify the term of "species complex" within the review.

R: We agreed with this comment, we added the following sentence in the text “In the literature, the term "species complex" can have different meanings, ranging from the complexity of the taxonomic dissection of what a species name encompasses (taxonomic species complex), to "complex diseases" where many species are associated with the disease (co-occurrence), without understanding which actually are the causal agent(s) and which are microbial species systematically associated with the disease without playing a role in the infection or exploiting the symptoms as secondary invaders. In other cases, such as leaf blotch in wheat, it is a set of species associated with a disease that is replaced over time or as a function of the geographical distribution of the host and/or pathogen. Taken together, three kinds of species complexes can be defined: (i) disease complexes with pathogens coexisting on different ecological niches and without any physically interaction, (ii) disease complexes where association between different species is the norm, but the impact of each pathogen remains unknown, and (iii) actual disease complexes, where there is at least minimal evidence of the involvement of more than one species in disease severity”

 

There is language not in English in Figure 1.

R: Correction done

Introduce species with their full scientific names upon first mention, such as C. musae, L. maculans, P. pinodella….

R: Correction done

The biggest problem I find in this article: Figure 2 should be closely linked to the corresponding content: The link between Fig 2 and 5.1, 5.2, 5.3, 5.4…is not tight; The direct/indirect effects are not clear; It is suggested that every point in Fig 2 should be connected well to the content.

R: We agreed with this comment, we added sentence to connect the text with this figure

First appearance of abbreviation should include the full name of the term, such as LAI, IPM; check the entire article. And why LHT is only appear in the abstract?

R: Correction done. We detailed all the abbreviation, and remove the LHT from the abstract section, as it is not necessary

Reviewer 4 Report

Comments and Suggestions for Authors

The manuscript ID: Agronomy -2980008 “Consideration of the disease complexes, the missing link to cor rectly analyze the impact of intercropping on disease development” has been reviewed.

I this review the authors showed a significant regarding intercropping as an interesting way to stabilize yields and reduce disease risk. In this review, the authors focused on fungal leaf diseases and described: the mechanisms that contribute to disease clustering and that drive interactions, but also reviewed strategies that foliar diseases to deal with these co-infections;  how intercropping can lead to changes in epidemic dynamics; presented the approach that should be taken to properly test intercropping in a multiple infection situation.

This is  interesting paper, however, I have a few comments :

In the Introduction add a description of tillage sysyems, that also affect the infection of plants by pathogens.

In the Introduction add how the immune system of the host plant responds to infection (the main mechanisms of plant resistance to pathogens).

The text of the manuscript requires corrections, including the completion of the full Latin names.

Figure 1 needs to be corrected (there are parts of English and French descriptions).

Under Figure 1 is given (adapted from Rynkiewicz et al. 2023), but such an item is not in References, is instead Rynkiewicz et al. 2015.

In my opinion, the authors for this review used a lot of old literature on the subject (there are important information), but in the current situation the paper needs to be supplemented with more recent data from the last years of research2018-2024.

Incorrectly prepared citations: given authors, and there should be numbers of cited literature (e.g. Tilman 1999 [2]; Gliessman 2001 [3] …..

Literature in References given alphabetically, and should be in order of citation [1, 2, 3, 4, ….]

Lack of line numbering in the manuscript , which makes it difficult to evaluate the review. Therefore, I have highlighted comments in the text of the manuscript.

Comments for author File: Comments.pdf

Author Response

This is interesting paper, however, I have a few comments :

In the Introduction add a description of tillage sysyems, that also affect the infection of plants by pathogens.

R: We agreed with this comment, we added the following sentence :” Tillage systems are sequences of operations that manipulate the soil in order to produce ac rop. Operations include tilling, plating, fertilization, pesticide application, harvesting and residue chopping. All these operations can modify the dynamics and the structure of the canopy. More particularly, crop residue management is particularly important to manage for necrotrophy pathogen that are able to survive on stubbles.  

In the Introduction add how the immune system of the host plant responds to infection (the main mechanisms of plant resistance to pathogens).

R: We agreed with this comment, however we think that it is more appropriate to add this explanation in the 5.2 section. we added the following sentence: “Many plant-associated microbes are pathogens that impair plant growth and reproduction. Plants respond to infection using a two-branched innate immune system. The first branch recognizes and responds to molecules common to many classes of microbes, the second branch responds to pathogen virulence factors, either directly or through their effects on host targets.

The text of the manuscript requires corrections, including the completion of the full Latin names.

R: Correction done

Figure 1 needs to be corrected (there are parts of English and French descriptions).

R: Correction done

Under Figure 1 is given (adapted from Rynkiewicz et al. 2023), but such an item is not in References, is instead Rynkiewicz et al. 2015.

R: It is a mistake, correction done

In my opinion, the authors for this review used a lot of old literature on the subject (there are important information), but in the current situation the paper needs to be supplemented with more recent data from the last years of research2018-2024.

R: As a reminder, in this review we have chosen to focus on foliar diseases of fungal origin. Further to this comment, we have carried out a review of the literature on the impact of intercropping on the development of diseases. After analysis, it appears that there are very few articles dealing with foliar diseases due to fungal pathogens. Most of the publications concern soil-borne diseases and pests. Concerning the literature used in this review, 39% of the literature was published between 2018 and 2024.

Incorrectly prepared citations: given authors, and there should be numbers of cited literature (e.g. Tilman 1999 [2]; Gliessman 2001 [3] …..

R: Correction done

Literature in References given alphabetically, and should be in order of citation [1, 2, 3, 4, ….]

R: Correction done