Puccinia Spore Concentrations in Relation to Weather Factors and Phenological Development of a Wheat Crop in Northwestern Spain

Round 1

Reviewer 1 Report

Dear authors,

While the research is interesting and it seems to be a great point for the agriculture in Spain.

You spend the most explaining how the meteorological parameters affect to the puccinia concentrations in the full phenological season and by the duration of each growth stages but you do not explain why is important to know the correlation by stage.

While the model use in the last part has been descrived in a previous paper it will be better to include the comparison between the days predicting leaf rush and your Puccinia concentrations.

Apart od that I have only a few coments about the manuscripipt:

Material and methods

line 125 : instead of "Rodriguez Moreno et al. [9], with modifications was tested" write "Rodriguez Moreno et al. [9],  was tested with modifications"

line 167: include an space in "observedat the fruit development stage"

line 231: as you are describing only the significant correlations include significant in : "year 2022 showed a significant positive degree of association"

 

Author Response

The authors are grateful for the suggestions and comments on the article “Puccinia spore concentrations in relation to weather factors and phenological development of a wheat crop in Northwestern Spain”, which contribute to improve its quality. We resubmit our manuscript after addressing the comments below.

1. While the research is interesting and it seems to be a great point for the agriculture in Spain. You spend the most explaining how the meteorological parameters affect to the Puccinia concentrations in the full phenological season and by the duration of each growth stages but you do not explain why is important to know the correlation by stage.

Response/ The correlations by phenological stages allowed us to demonstrate that although some meteorological variables had no relationship with the total concentrations of Puccinia in the air, they influenced its presence at some time during the growing season. This was the case, for example, in the year 2021 with relative humidity, wind speed, hours of sunshine, and leaf moisture.

The following paragraph was added regarding the wind speed variable, which had not been addressed in detail in the discussion:

The correlation between Puccinia concentrations and wind speed was positive in most of the phenological stages where it was detected, as well as in 2022 with total concentrations. Similar results have been obtained by other researchers, who point out that this correlation varies depending on wind direction [30]. The influence of this meteorological variable may favor the dispersion of fungal propagules over long distances, and spores from other regions may be detected. Hovmøller et al. [39] reported that Puccinia striiformis f.sp. tritici, the cause of wheat stripe rust, migrates frequently between the United Kingdom, Germany, France, and Denmark. Additionally, they demonstrated through a phylogeographic analysis the existence of a single clonal population of this species in the four countries, separated by a distance of up to 1,700 km.

2. While the model use in the last part has been described in a previous paper it will be better to include the comparison between the days predicting leaf rush and your Puccinia

Response/ The authors considered that taking into account the data collected and the results of Spearman's correlation and the PCA, the most appropriate model to apply was that of Rodriguez Moreno et al. (2020), which takes into account the meteorological variable temperature. Additionally, other research studies in the northern hemisphere have shown that temperature is the main factor influencing the dynamics of Puccinia. The idea suggested by the reviewer is very interesting and will be taken into account in future work.

Apart of that I have only a few comments about the manuscript:

Material and methods

3. Line 125: instead of "Rodriguez Moreno et al. [9], with modifications was tested" write "Rodriguez Moreno et al. [9], was tested with modifications"

Response/ This error has been corrected.

4. Line 167: include a space in "observedat the fruit development stage"

Response/ This error has been corrected.

Line 231: as you are describing only the significant correlations include significant in: "year 2022 showed a significant positive degree of association"

Response/ This recommendation was accepted.

Reviewer 2 Report

The authors presented data on the number of spores in relation to the wheat phenology, but they didn't provide any information on the progress of rust in the Caaveiro wheat plantation. The data on rust progress in the field is an important aspect that would help improve the article's clarity and provide a more comprehensive understanding of the study.

No comments

Author Response

The authors are grateful for the suggestions and comments on the article “Puccinia spore concentrations in relation to weather factors and phenological development of a wheat crop in Northwestern Spain”, which contribute to improve its quality. We resubmit our manuscript after addressing the comments below.

Comment: The authors presented data on the number of spores in relation to the wheat phenology, but they didn't provide any information on the progress of rust in the Caaveiro wheat plantation. The data on rust progress in the field is an important aspect that would help improve the article's clarity and provide a more comprehensive understanding of the study.

Response/ The aspect he highlights is very interesting, and we can consider it for future research. Field studies can be examined from various perspectives, and our goal was to determine the concentrations of Puccinia in the air and their relationship with meteorological variables during the different phenological stages of wheat cultivation. Achieving this objective helps us comprehend the aerobiology of the genus in this region, as there is no prior study on this subject. Such aeromycological studies are highly significant as they allow farmers to be informed about the presence of phytopathogens in the air before leaf lesions occur, reducing the likelihood of infection in susceptible plants when environmental conditions are conducive to their development.

Reviewer 3 Report

Thank you for the opportunity to review this paper. The manuscript is certainly useful; some of the issues need to be taken care of:

1.      First, In the Introduction there should be some statistics specifically about the production of wheat in Spain and its role in the economy.

2.      Second, in the discussion write a few sentences about the uncertainties in modeling changes in disease spread, if any.

3.      Lastly, Please show the results of wheat spores identification, you can provide them as supplementary materials

Specific comments

1.      Line 252, First mention then use abbreviate.

2.      Line 360, add a couple of references to support rainfall's effect on disease incidence.

 

3.      Line 362-363, please revise the sentence's syntax. 

Author Response

The authors are grateful for the suggestions and comments on the article “Puccinia spore concentrations in relation to weather factors and phenological development of a wheat crop in Northwestern Spain”, which contribute to improve its quality. We resubmit our manuscript after addressing the comments below.

Comments and Suggestions for Authors

Thank you for the opportunity to review this paper. The manuscript is certainly useful; some of the issues need to be taken care of:

1. First, In the Introduction there should be some statistics specifically about the production of wheat in Spain and its role in the economy.

Response/ This recommendation was accepted and added the following paragraph:

According to the records of the Food and Agriculture Organization of the United Nations (FAO), in the year 2021, Spain's wheat production amounted to 8,564,630 tons, and it im-ported 4,017,657.85 tons to cover national demand [2]. Bread is one of the main foods produced with this cereal in the country, and Spanish households spend 4.41% of their total expenditure on food and beverages for home on the purchase of this product. Each Spanish individual consumes an average of 30.07 kilos of bread per year [3].

• [2] Food and Agriculture Organization of the United Nations. Available online: https://www.fao.org/faostat/en/#data/QCL (accessed 4 August 2023).
• [3] Ministerio de Agricultura, Pesca y Alimentación. (2021). Informe de Consumo Alimentario en España 2021. Available online: https://www.mapa.gob.es/es/alimentacion/temas/consumo-tendencias/informe-consumo-alimentario-2021-baja-res_tcm30-624017.pdf (accessed 4 August 2023).

2. Second, in the discussion write a few sentences about the uncertainties in modeling changes in disease spread, if any.

Response/ The model of Rodriguez-Moreno et al. (2020) is designed to predict the occurrence or non-occurrence of Puccinia rust, taking into account the values of average temperature, nighttime temperature, and dew point temperature. The adjustment we made was to change the range of nighttime temperature hours from 20:00 - 7:00 to 23:00 - 7:00 because, during the study period, it is still daylight at 20:00. To make this information clearer, we added the following sentence:

For this purpose, we modified the range of nighttime temperature hours from 20:00 - 7:00 to 23:00 - 7:00, based on the climatic conditions of the study area during this period when it gets dark later.

In addition, we add in the table the following clarification about the time range found in the table 4:

* Nocturnal temperature of the Rodriguez-Moreno et al. (2020) model.

3. Lastly, Please show the results of wheat spores identification, you can provide them as supplementary materials

Response/ This recommendation was accepted and the information requested in Figure S1 was added.

Specific comments

1. Line 252, First mention then use abbreviate.

Response/This recommendation was accepted.

2. Line 360, add a couple of references to support rainfall's effect on disease incidence.

Response/This recommendation was accepted and added the following references:

• Nagarajan S. U. L. P. H. U. R.; Singh D. V. Long-distance dispersion of rust pathogens. Annual review of phytopathology 1990, 28, 139-153.
• Geagea L.; Huber L.; Sache I.; Flura D.; McCartney H. A.; Fitt B. D. Influence of simulated rain on dispersal of rust spores from infected wheat seedlings. Agricultural and Forest Meteorology 2000, 101, 53-66.

3. Line 362-363, please revise the sentence's syntax.

Response/This recommendation was accepted and the indicated sentences were corrected.

The analysis of the combined effect of all meteorological variables on Puccinia concentrations enabled us to ascertain that in the year 2022, hours of sunshine and relative humidity also played a significant role in its detection. An increase in sunshine hours leads to higher temperatures, which are suboptimal for Puccinia development. On the other hand, relative humidity is known to be the primary factor influencing the development of leaf rust in wheat [35]. High humidity is optimal for stripe rust infection [36], while lower humidity promotes the spread of stem rust, which could have been predominant in 2021 and explains the negative association with humidity [37].

 

Reviewer 4 Report

1. What is the main question addressed by the research?

R: The authors have determined the temporal variation of airborne spores of Puccinia and their relationship with meteorological variables and the phenological development of a wheat crop in Northwestern Spain during two growing seasons.
2. Do you consider the topic original or relevant in the field? Does it
address a specific gap in the field?

R: Yes the topic is original and it could be beneficial research at a specific regional scale.
3. What does it add to the subject area compared with other published
material?

R: There are no records of aero mycological studies in Spanish wheat fields for the identification and quantification of Puccinia spores in different growing seasons. This is the only novelty of the present study.
4. What specific improvements should the authors consider regarding the
methodology? What further controls should be considered?

R: Though, the methodology is written well, however, it lacks information about crop management practices and authors must include this information in the revised version.
5. Are the conclusions consistent with the evidence and arguments presented
and do they address the main question posed?

R: Yes conclusion is consistent with the evidence and they are addressing the posed questions.
6. Are the references appropriate?

R: Yes they are appropriate.
7. Please include any additional comments on the tables and figures.

R: The quality of the figures must be improved, and the size of the text and legend in the figures must be made visible to readers.

 

The work carried out is an interesting idea and it is providing very useful results. However, a few changes are needed before final publication.

The abstract is poorly written as it is currently covering the methodology of the study. The study findings are not well explained in this section, therefore, I suggested the authors to add core study findings and then add a solid conclusion at the end of the abstract section.

I also suggest the authors to improve the readability of the text starting from the abstract to the conclusion section.

In the introduction section authors can add more information about the importance of wheat in terms of production and nutrition.

Before objectives, authors can add a strong hypothesis of their study findings.

How this study could be beneficial at a global scale, as it is covering specific regions and this disease vary in different climatic regions.

The quality of figures is very poor, therefore figures must be made clear and visible to readers.

The discussion section is written well, however, it still needs to be enriched with cool logical reasoning.

 

 

 

 

 

 

 

Minor English changes are needed 

Author Response

The authors are grateful for the suggestions and comments on the article “Puccinia spore concentrations in relation to weather factors and phenological development of a wheat crop in Northwestern Spain”, which contribute to improve its quality. We resubmit our manuscript after addressing the comments below.

The work carried out is an interesting idea and it is providing very useful results. However, a few changes are needed before final publication.

1. The abstract is poorly written as it is currently covering the methodology of the study. The study findings are not well explained in this section, therefore, I suggested the authors to add core study findings and then add a solid conclusion at the end of the abstract section.

Response/ This recommendation was accepted and the summary was modified taking into account the suggestion.

Rust is one of the main diseases affecting wheat crops in Spain, causing significant yield and quality losses. Research on its identification and quantification in the air is a worldwide priority due to the importance of this crop as a source of food and feed. The objective of this study is to determine the temporal variation of airborne spores of Puccinia and their relationship with me-teorological variables and the phenological development of a wheat crop in Northwestern Spain during two growing seasons. The study was conducted in A Limia, Ourense, located in North-western Spain, during the wheat growing seasons of 2021 and 2022. The Lanzoni VPPS 2010 spore trap was used to collect airborne spores, which were identified by optical microscopy. The wheat growing season was less than 95 days during both years, and wheat rust spores were detected during all phenological stages of the crop. Concentrations were higher than 100 spores/m3 from the booting stage to senescence, mainly in 2021. Statistical analyses showed that temperature was the meteorological variable that most influenced Puccinia concentrations in the air in both years. Modification of a prediction model proposed by other authors for wheat rust, which takes into account mean temperature (10-25 °C), dew point temperature (<5 °C), and nighttime temperature (10-20 °C), allowed us to tentatively predict the increase of Puccinia concentrations in the year 2022 when these conditions occurred for four or five consecutive days. This research is the first in Spain to report the presence of rust-causing Puccinia spores in the air during all phenological stages of the wheat crop and provides useful information for designing management strategies, considering temperature values.

2. I also suggest the authors to improve the readability of the text starting from the abstract to the conclusion section.

Response/ This recommendation was accepted and the readability of the text was improved.

3. In the introduction section authors can add more information about the importance of wheat in terms of production and nutrition.

Response/ This recommendation was accepted and added the following paragraph:

According to the records of the Food and Agriculture Organization of the United Nations (FAO), in the year 2021, Spain's wheat production amounted to 8,564,630 tons, and it imported 4,017,657.85 tons to cover national demand. Bread is one of the main foods produced with this cereal in the country, and Spanish households spend 4.41% of their total expenditure on food and beverages for home on the purchase of this product. Each Spanish individual consumes an average of 30.07 kilos of bread per year.

• Food and Agriculture Organization of the United Nations. Available online: https://www.fao.org/faostat/en/#data/QCL (accessed 4 August 2023).
• Ministerio de Agricultura, Pesca y Alimentación. (2021). Informe de Consumo Alimentario en España 2021. Available online: https://www.mapa.gob.es/es/alimentacion/temas/consumo-tendencias/informe-consumo-alimentario-2021-baja-res_tcm30-624017.pdf (accessed 4 August 2023).

4. Before objectives, authors can add a strong hypothesis of their study findings.

Response/ This recommendation was accepted and added the following paragraph:

Our study is intended to demonstrate that rust-causing Puccinia spores are present in the air during the different phenological phases of wheat cultivation in Northwestern Spain and that their concentrations are affected by meteorological variations.

5. How this study could be beneficial at a global scale, as it is covering specific regions and this disease vary in different climatic regions.

Response/ Although this study covers a specific region, it is relevant worldwide because rust-causing Puccinia spores are dispersed by wind over long distances. Hovmøller et al. (2002) reported that Puccinia striiformis f.sp. tritici, the cause of wheat stripe rust, migrates frequently between the United Kingdom, Germany, France, and Denmark. Additionally, they demonstrated through a phylogeographic analysis the existence of a single clonal population of this species in the four countries, separated by a distance of up to 1,700 km. Justesen et al. (2002) suggested that prevailing winds from the south or west caused the reappearance of airborne spores of Puccinia striiformis f.sp. tritici at locations in Denmark in 1997.

Seasonal movement of wheat stem rust urediospores from northern Mexico/Texas to the U.S./Canada border has also been shown in the Americas. In the fall, urediospores of P. graminis tritici from wheat fields around the Great Lakes move to Texas (Northern Mexico) at the same time that the monarch butterfly (Danaus plexippus) migrates south to its winter habitat (Nagarajan et al., 1990).

The long-distance migration of pathogen clones, coupled with low host species diversity, may render previously useful resistance genes ineffective for disease control on a continental scale.

Some of these ideas were used in the discussion section.

• Hovmøller M. S.; Justesen A. F.; Brown J. K. M. Clonality and long‐distance migration of Puccinia striiformis sp. tritici in north‐west Europe. Plant pathology 2002, 51, 24-32.
• Justesen A. F.; Ridout C. J.; Hovmøller M. S. The recent history of Puccinia striiformis sp. tritici in Denmark as revealed by disease incidence and AFLP markers. Plant pathology 2002, 51, 13-23.
• Nagarajan S. U. L. P. H. U. R.; Singh D. V. Long-distance dispersion of rust pathogens. Annual review of phytopathology 1990, 28, 139-153.

6. The quality of figures is very poor, therefore figures must be made clear and visible to readers.

Response/ The recommendation was accepted and the quality of the figures was improved. Also they are in a separate .zip file with the resolution required by the journal.

7. The discussion section is written well, however, it still needs to be enriched with cool logical reasoning.

Response/ The recommendation was accepted and some ideas were added to this section.

In addition, information on crop management practices was included in the results.

 

 

 

 

 

Round 2

Reviewer 1 Report

Dear authors,

The work conducted in the present manuscript has led to significant improvements.

First and foremost, I would like to express my appreciation for the authors' decision to incorporate Figure S1. This addition is instrumental in enabling readers to discern the spores under investigation.

My primary concern pertains to the concluding statement: "the peaks occurred at the same phenological stages and were detected throughout the growing season." Regrettably, this assertion is inaccurate. The analysis reveals that the peaks, accompanied by higher concentrations based on the stages, materialized in 2021 during the fruit development stage (S7) and in 2022 during the ripening of fruits and seeds stage (S8). Therefore, I strongly recommend the exclusion of this particular sentence from the concluding remarks.

 

Author Response

Thank you very much for your comments. The sentence you suggested to delete was removed from the conclusions.

Reviewer 3 Report

Thank you for addressing all the concerns adequately. The ms could be accepted now

Author Response

Thank you very much for your comments.

Reviewer 4 Report

The authors have improved the manuscript as per my suggestions. Therefore, it can be accepted for publication now. 

Minor changes are needed 

Author Response

Thank you very much for your comments.