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Research Article
Revised

Rice plants reduce methane emissions in high-emitting paddies

[version 2; peer review: 3 approved with reservations]
Previously titled: Rice cultivation reduces methane emissions in high-emitting paddies
PUBLISHED 27 Jun 2019
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This article is included in the Agriculture, Food and Nutrition gateway.

Abstract

Background: Rice is understood to enhance methane emissions from paddy fields in IPCC guidelines. However, rice actually has two separate functions related to methane: i) emission enhancement, such as by providing emission pathways (aerenchyma) and methanogenetic substrates; and ii) emission suppression by providing oxygen pathways, which suppress methanogenesis or enhance methane oxidation. The overall role of rice is thus determined by the balance between its enhancing and suppressing functions. Although previous studies have suggested that rice enhances total methane emissions, we aimed to demonstrate in high-emitting paddy fields that the overall methane emission is decreased by rice plants.
Methods: We compared methane emissions of with and without rice plants in triple cropping rice paddies in the Mekong Delta, Vietnam. The gas samples are collected using chamber method and ware analyzed by gas chromatography.
Results: We found that rice, in fact, suppressed overall methane emissions in high-emitting paddies. The emission reductions increased with the growth of rice to the maximum tillering stage, then decreased after the heading stage, and finally recovered. 
Discussion:  Our result indicates that the overall methane emission by ebullition is larger than the overall emission of rice planted area. In addition, although many studies in standard-emitting paddies have found that the contribution of soil organic matter to methanogenesis is small, our results in high-emitting paddies suggest that methanogenesis depended mainly on soil organic matter accumulated from past crops. The higher the methane emission level, the lower the contribution of the rice-derived substrate; therefore, the role of rice in high-emitting paddies is the opposite to in that of standard-emitting paddies.
Conclusion: The present study demonstrates that during the growing season, rice is suppressing methane emissions in high-emitting paddies. This means the significance of using the rice variety which has high suppressing performance in high-emitting paddies.

Keywords

Greenhouse gases, Mekong Delta, Methane oxidation, Methanogenesis inhibition, Rice paddy, Triple cropping

Revised Amendments from Version 1

  1. Title: The term changed from “cultivation” to “plants” as more suitable to the content.
  2. The aim of the study was more clarified.
  3. The terms changed to be consistent.
  4. The unclear expressions or grammatical mistakes were corrected.
  5. The wrong words were corrected as follows. “rice providing” -> “rice-derived”, “other plots”-> “other points”, “230 g m −2” -> “230 kg ha −1”.
  6. A recent reference (Jiang et al., 2017) which supported our conclusion was added.
  7. The consideration for the plant density on the effect of early stage rice to methane emission was added.
  8. The consideration for the effect of ebullition on the high emission in the initial stage methane emission was added.
  9. Figure 2 was revised-the labels have been corrected from "Non Rice" to "No Rice".
  10. The formula of methane emission reduction rate was added in the main sentence.
  11. The conclusion section was added and the impact of the study was mentioned.

See the authors' detailed response to the review by Azeem Tariq
See the authors' detailed response to the review by Dung Duc Tran
See the authors' detailed response to the review by Kees Jan van Groenigen

Introduction

The role of rice in methane (CH4) emissions changes according to emission levels. Rice performs three key functions related to CH4 emissions: i) providing a CH4 pathway through a well-developed system of intercellular air spaces (aerenchyma), ii) providing a substrate for methanogenesis, and iii) oxidizing CH4 in rhizosphere by supporting O2 counter-transport through aerenchyma system16. The level of contribution of these functions varies with the overall emissions, and the total amount of CH4 emitted to the atmosphere is thus a balance between CH4 production and oxidation6. To the best of our knowledge, rice enhances overall CH4 emissions from paddy fields. In addition, previous studies have mostly disregarded a potential impact of overall emission levels on the role of rice in enhancing or suppressing CH4 emissions.

Cicerone and Shetter measured CH4 emissions with a closed chamber on the water surface of a paddy field, and found that 4 hours after starting measurement, CH4 concentration was 290 ppm over rice plants and only 4 ppm over open water1. Further studies have revealed that CH4 produced under methanogenesis diffuses through the soil, which is oxidized by the surface barrier before reaching the atmosphere2,7. Rice absorbs diffused CH4 from its roots and emits CH4 through aerenchyma3,5,7. Therefore, an established theory has emerged that CH4 is not emitted from the soil without rice. Other recent studies have provided additional evidence that the primary source of CH4 is current-season photosynthates—specifically, root exudates or decaying tissues811. This results in CH4 emissions that peak during the late stage of rice growth. Thus, the presence of rice plants has been determined to be the cause of CH4 emissions in paddy fields.

Wassmann et al.12 measured CH4 emissions on the water surface of a paddy field amended with organic matter. They found that organic matter incorporation increased total CH4 emission levels from 27–90 to 160–240 kg CH4 ha−1 crop−1, and ebullition increased from 15–23% to 35–62%, respectively12. Since it is known that organic matter incorporation causes CH4 emissions to peak during the early stages of rice growth, when the rice is still small and the aerenchyma is not well developed, the results of Wassmann et al.12 should be closely examined to determine whether ebullition increased with total emissions. According to the 2006 Intergovernmental Panel on Climate Change (IPCC) guidelines, CH4 emissions for 100 days of rice cropping are 130 kg CH4 ha−1 crop−1; however, emissions were observed at almost twice this value by Wassmann et al.12 Average CH4 emissions from rice paddies in Asia without and with organic matter incorporation ranged from 16 to 200 and 250 to 500, respectively13. Although ebullition has been little studied14, ebullition must occur at high emission levels. Furthermore, in the study by Wassmann et al.12, twin CH4 emissions peaks appeared, with an early peak corresponding to the organic matter amendment and a later peak corresponding to rice-originated substrate12. An alternate interpretation of these results is that the twin peaks could reflect the oxidation performance of rice, since CH4 oxidation is known to increase with rice growth, up to the maximum tillering stage, and then decrease15.

We monitored CH4 emissions in the paddy fields for 5 years (total 15 crops) in triple rice cropping fields in the Mekong Delta, Vietnam. The CH4 emission level was an order of magnitude higher than IPCC standards. These high CH4 emissions suggest that ebullition must have been occurring. We thought there was a possibility that rice plants decrease overall methane emission based on the extremely high emission levels. It will be epochal if present the fact that rice plants decrease overall methane emission in paddy fields.

Results and discussion

We compared CH4 emissions with (Rice) and without rice (No Rice) on the water (soil) surface of paddy fields. Our results showed that rice decreased CH4 emissions by half of No Rice. The effect of rice was large even in the early growth stage because of the high plant density (230 kg ha−1 in dry weight; approximately 3 cm interval) and the rapid growth in the tropical climate (see Figure 1, Figure 2). Although the high CH4 emission is shown in the first week, it is considered to be caused by the erratic character of “ebullition”. In fact, there was no difference in the emission between Rice and No Rice on both the 7th and 9th day (see Figure 1). Complete, unprocessed data are available on figshare16. There was no marked CH4 emissions peak in the late-stage of the rice mentioned in previous studies811. This suggests that the amount of methanogenesis from the rice-derived substrate is relatively small. Note the high emission levels (500–1400 kg CH4 ha−1 crop−1). These findings suggest that total CH4 emissions are reduced by oxidation or methanogenesis inhibition associated with growing the rice plant.

624be410-2103-49f3-a2b3-4849d254f9ab_figure1.gif

Figure 1. Seasonal CH4 emissions in paddy fields.

Average CH4 emissions of rice-planted areas and no-rice-planted areas in triple cropping rice fields in the Mekong Delta. Winter–Spring season (2017). The paddy fields did not receive rice straw incorporation. Error bars are s.d. (n = 3).

624be410-2103-49f3-a2b3-4849d254f9ab_figure2.gif

Figure 2. Cumulative CH4 emissions in paddy fields.

Cumulated CH4 emissions of rice-planted areas and no-rice-planted areas in triple cropping rice fields in the Mekong Delta. The number in the legend relates to the fields.

We also found that the reduction rate of CH4 emissions increased with the growth of the rice plant. The CH4 reduction rate was calculated using a moving average of five values by the following formula.

  • reduction rate = (No Rice – Rice)/No Rice

The rate peaked at maximum tillering stage, then bottomed at after heading stage, and then recovered (see Figure 3). The decrease around the heading stage was caused partially by an increase of emissions in rice-planted areas, and mainly by the erratic emissions in the unplanted area.

624be410-2103-49f3-a2b3-4849d254f9ab_figure3.gif

Figure 3. Reduction rate of CH4 emissions.

The CH4 reduction rate was calculated by (No Rice – Rice)/No Rice.

No consensus has yet been reached on the extent to which methanotrophs or rice roots attenuate CH4 emissions17. Using the N2 atmosphere technique, CH4 oxidation ratios have been found to be around 40% on average and were relatively stable throughout the rice growing season17. However, genuine CH4 oxidation, as measured using inhibitors, tend to decrease with rice growth, and the reduction rate for total CH4 emissions can reach up to 20%17. Although, most of those studies assume plant-mediated transportation17, in general, our results roughly matched the results using the N2 atmosphere technique. This suggests that the reduction in CH4 emissions is not due to genuine oxidation and is more likely to be due to methanogenesis inhibition by oxygen from aerenchyma, which lasts until harvesting18.

We found high CH4 emissions in unplanted paddy fields of which not incorporate organic materials. Despite this lower input of methanogenesis substrate, CH4 emission levels were 12 times higher than the IPCC guidelines. The emission levels remained almost stable after reaching a maximum. This suggests that methanogenesis mainly depends on soil organic matter that has been accumulated from past rice crops. Prior studies have suggested that the contribution of soil organic matter to methanogenesis is small; however, these studies also indicated that higher emission levels tend to be associated with higher contribution rates of soil organic matter811,19. Furthermore, a recent study found that large rice plants reduce CH4 emissions compared to small rice plants in paddy fields with high soil C contents; instead, they show the opposite effect in paddies with low soil C contents20. Thus, our results are consistent with prior studies that assume that emission levels are proportional to the amount of soil organic matter which can be a methanogenesis substrate.

High-emitting paddies of CH4 emissions, which exist widely across tropical Asia, would have huge soil organic matter stock formed by sequential rice cropping under flooded conditions. For instance, the use of a rice variety which has better performance of methanogenesis inhibition in high-emitting paddies is very effective; the 10 % reduction is equivalent to 100% of methane emission in standard paddy fields. On the other hand, without rice plants, the methane emission from the existing soil organic matter stock will double by ebullition; the 100% increase is equivalent to 1000% of the standard paddies. This suggests that the future study for the soil organic matter stock map is critical.

Conclusion

Most studies of CH4 emissions in paddy fields have been conducted in fields with low overall emission levels. Since the role of rice in CH4 emissions varies according to the overall emission levels, these results cannot be appropriately generalized to rice paddies with high emission levels. The results of our study suggest that rice reduces emissions in high-emitting paddies. The emission levels are related to the amount of soil organic matter which can be a methanogenesis substrate; this suggests that the future study for the soil organic matter stock map is critical.

Methods

Study site

Experimental fields were in Tan Loi 2 Hamlet, Thuan Hung village, Thot Not district, Can Tho city, Vietnam. Farmers conduct triple rice cropping by direct seeding and full flooding. This district receives almost 2 months of a flood annually from the Mekong River. The flood decomposes rice straw underwater to the extent that it is no obstacle for seeding. Therefore, farmers start the rice cropping by leveling the fields, without incorporating rice straw. We observed CH4 emissions in 18 paddy fields (26 × 17 m each) under several conditions for 5 years from September 2011. A preliminary study was conducted with the rice variety OM501 (suitable for the season) in the Summer-Autumn season of 2016 by the same methods and paddies of the present study (see Figure 4). In the present study, we used three fields for replication. We conducted the present study after the annual flood (4 November 2016–12 February 2017); these fields did not incorporate rice straw because of the period was after the annual flood.

624be410-2103-49f3-a2b3-4849d254f9ab_figure4.gif

Figure 4. Seasonal CH4 emission in paddy fields.

Average CH4 emissions of rice-planted areas and no-rice-planted areas in triple cropping rice fields in Mekong Delta. Summer–Autumn season (2016). The paddy fields received incorporated rice straw of the previous crop. Error bars are s.d. (n = 3).

Treatment

We compared CH4 emissions with (Rice) and without rice (No Rice). We set 2 × 2 m squares of plastic films on a part of each three fields just before seeding, then carefully removed them with seeds on the films immediately after seeding. In other points, there was no difference with farmers’ conventional rice-growing procedures. Farmers scattered 230 kg ha−1 (in dry weight) of germinated rice seed (variety Jasmine) on drained wet paddy fields’ surfaces on 5th November. This wet condition was maintained for 7 days, then the fields were kept flooded until 89 days after seeding (DAS), and the rice harvested on 100 DAS. The farmers applied fertilizer, which included 76 kg of urea on 12 November, 53 kg each of urea and NPKS (16-16-8-13), diammonium phosphate on 19 November, and 53 kg each of urea and NPKS on 15 December. The daily average water levels were monitored with water level loggers (HOBO U20; Onset Computer Corporation, Bourne, Massachusetts) at the corner of the fields, and the average levels were 2.0 cm (−0.6 to 6.1 cm) until drained.

Measurement of CH4 emissions

We set an approximately 2 m long and 0.5 m wide ladders from the center of the shorter bund to allow measurement of CH4 without touching the paddy soil surface. Those ladders were on the borders of the non-planted areas in each field. We set PVC chamber bases on the paddy fields of both sides of the ladders to avoid measurement perturbation. Chambers (60 × 80 cm and 100 cm high, transparent acryl) were set on a watertight chamber bases for every measurement. Measurements were taken at 8 a.m. because previous research has indicated that emissions at this time have a high correlation (ca. 90% of average emission) with average daily emissions21. We mixed the air in the chamber with a fan for 5 min after setting the chamber, then sampled the first gas, then sampled the second gas 20 min later. We conducted the measurements once a week throughout the rice growing stage, but every 3 days for 2 weeks after seeding, heading stage, and around draining. The samples were analyzed by gas chromatography (GC-14B, Shimazu, Kyoto). The cumulative CH4 emissions were calculated by linear interpolation.

Ethics statement

This study was conducted with the approval of the farmer.

Statistical analysis

Data were processed using Microsoft Excel 2016.

Data availability

Raw data of this article is available from figshare: https://doi.org/10.6084/m9.figshare.6916277.v116. Data 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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Version 3
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Oda M and Nguyen Huu C. Rice plants reduce methane emissions in high-emitting paddies [version 2; peer review: 3 approved with reservations]. F1000Research 2019, 7:1349 (https://doi.org/10.12688/f1000research.15859.2)
NOTE: If applicable, it is important to ensure the information in square brackets after the title is included in all citations of this article.
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ApprovedThe paper is scientifically sound in its current form and only minor, if any, improvements are suggested
Approved with reservations A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit.
Not approvedFundamental flaws in the paper seriously undermine the findings and conclusions
Version 2
VERSION 2
PUBLISHED 27 Jun 2019
Revised
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Reviewer Report 09 Jul 2019
Dung Duc Tran, Center of Water Management and Climate Change (WACC), Vietnam National University – Ho Chi Minh City (VNU – HCM), Ho Chi Minh City, Vietnam 
Approved with Reservations
VIEWS 11
The manuscript has been improved based on the comments. However, I recommended the authors to consider the following 2 points before approval for indexing:
  1. The authors replied: "We corrected the method section and clarified the details.
... Continue reading
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HOW TO CITE THIS REPORT
Tran DD. Reviewer Report For: Rice plants reduce methane emissions in high-emitting paddies [version 2; peer review: 3 approved with reservations]. F1000Research 2019, 7:1349 (https://doi.org/10.5256/f1000research.21593.r50479)
NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article.
  • Author Response 25 Jul 2019
    Masato Oda, Crop, Livestock and Environment Division, Japan International Research Center for Agricultural Sciences, Tsukuba, 305-8686, Japan
    25 Jul 2019
    Author Response
    Thank you for the comment.

    1. For the site local map:

    We added the link to the Google map according to the article guidelines of F1000Research. The link takes no time for ... Continue reading
COMMENTS ON THIS REPORT
  • Author Response 25 Jul 2019
    Masato Oda, Crop, Livestock and Environment Division, Japan International Research Center for Agricultural Sciences, Tsukuba, 305-8686, Japan
    25 Jul 2019
    Author Response
    Thank you for the comment.

    1. For the site local map:

    We added the link to the Google map according to the article guidelines of F1000Research. The link takes no time for ... Continue reading
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22
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Reviewer Report 05 Jul 2019
Azeem Tariq, UMR 951 Innovation SupAgro-INRA-CIRAD, Montpellier SupAgro-IRC, Montpellier, France 
Approved with Reservations
VIEWS 22
I have checked the authors’ report. It is hard to follow the changes made by authors in ... Continue reading
CITE
CITE
HOW TO CITE THIS REPORT
Tariq A. Reviewer Report For: Rice plants reduce methane emissions in high-emitting paddies [version 2; peer review: 3 approved with reservations]. F1000Research 2019, 7:1349 (https://doi.org/10.5256/f1000research.21593.r50481)
NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article.
  • Author Response 25 Jul 2019
    Masato Oda, Crop, Livestock and Environment Division, Japan International Research Center for Agricultural Sciences, Tsukuba, 305-8686, Japan
    25 Jul 2019
    Author Response
    Thank you for reconsidering our manuscript. The methodology is described in the first sentence of the ‘Results and discussion’: “We compared CH 4 emissions with (Rice) and without rice (No ... Continue reading
COMMENTS ON THIS REPORT
  • Author Response 25 Jul 2019
    Masato Oda, Crop, Livestock and Environment Division, Japan International Research Center for Agricultural Sciences, Tsukuba, 305-8686, Japan
    25 Jul 2019
    Author Response
    Thank you for reconsidering our manuscript. The methodology is described in the first sentence of the ‘Results and discussion’: “We compared CH 4 emissions with (Rice) and without rice (No ... Continue reading
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Reviewer Report 04 Jul 2019
Kees Jan van Groenigen, Department of Geography, College of Life and Environmental Sciences, University of Exeter, Exeter, UK 
Approved with Reservations
VIEWS 19
While this revised version has improved, I still have some issues with this manuscript. Importantly, the comments by reviewer 1 weren't all fully addressed. Moreover, the manuscript contains many statements that are not supported by any references, and ideas that are not ... Continue reading
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HOW TO CITE THIS REPORT
van Groenigen KJ. Reviewer Report For: Rice plants reduce methane emissions in high-emitting paddies [version 2; peer review: 3 approved with reservations]. F1000Research 2019, 7:1349 (https://doi.org/10.5256/f1000research.21593.r50480)
NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article.
  • Author Response 25 Jul 2019
    Masato Oda, Crop, Livestock and Environment Division, Japan International Research Center for Agricultural Sciences, Tsukuba, 305-8686, Japan
    25 Jul 2019
    Author Response
    Thank you very much for your kind suggestion. Furthermore, thank you so much for correcting and improving the English. We completed the lack of references.
     
    We revised the manuscript for the ... Continue reading
COMMENTS ON THIS REPORT
  • Author Response 25 Jul 2019
    Masato Oda, Crop, Livestock and Environment Division, Japan International Research Center for Agricultural Sciences, Tsukuba, 305-8686, Japan
    25 Jul 2019
    Author Response
    Thank you very much for your kind suggestion. Furthermore, thank you so much for correcting and improving the English. We completed the lack of references.
     
    We revised the manuscript for the ... Continue reading
Version 1
VERSION 1
PUBLISHED 29 Aug 2018
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Reviewer Report 14 Jun 2019
Dung Duc Tran, Center of Water Management and Climate Change (WACC), Vietnam National University – Ho Chi Minh City (VNU – HCM), Ho Chi Minh City, Vietnam 
Approved with Reservations
VIEWS 12
The authors of "Rice cultivation reduces methane emissions in high-emitting paddies" present an interesting manuscript with great effort to demonstrate the balance between rice’s emitting and suppressing function changes according to overall methane emission levels. In general, the manuscript is ... Continue reading
CITE
CITE
HOW TO CITE THIS REPORT
Tran DD. Reviewer Report For: Rice plants reduce methane emissions in high-emitting paddies [version 2; peer review: 3 approved with reservations]. F1000Research 2019, 7:1349 (https://doi.org/10.5256/f1000research.17312.r48479)
NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article.
  • Author Response 27 Jun 2019
    Masato Oda, Independent Scientist, Japan
    27 Jun 2019
    Author Response
    Thank you very much for your precious suggestions. 

    1. We improved the abstract and the introduction to describe more clearly the aim of this study. 
    2. We corrected the method section and ... Continue reading
COMMENTS ON THIS REPORT
  • Author Response 27 Jun 2019
    Masato Oda, Independent Scientist, Japan
    27 Jun 2019
    Author Response
    Thank you very much for your precious suggestions. 

    1. We improved the abstract and the introduction to describe more clearly the aim of this study. 
    2. We corrected the method section and ... Continue reading
Views
24
Cite
Reviewer Report 28 May 2019
Kees Jan van Groenigen, Department of Geography, College of Life and Environmental Sciences, University of Exeter, Exeter, UK 
Approved with Reservations
VIEWS 24
Oda and Chiem present CH4 fluxes from Vietnamese rice paddies with- and without rice plants, and conclude that the presence of rice plants reduces CH4 emissions. Their results are interesting and convincing, and the experimental design seems solid. That said, ... Continue reading
CITE
CITE
HOW TO CITE THIS REPORT
van Groenigen KJ. Reviewer Report For: Rice plants reduce methane emissions in high-emitting paddies [version 2; peer review: 3 approved with reservations]. F1000Research 2019, 7:1349 (https://doi.org/10.5256/f1000research.17312.r46457)
NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article.
  • Author Response 27 Jun 2019
    Masato Oda, Independent Scientist, Japan
    27 Jun 2019
    Author Response
    1. Thank you for your precious suggestion! We changed the word "cultivation" to "plants" in the title. We think the word is more suitable to the content.
    2. Thank
    ... Continue reading
COMMENTS ON THIS REPORT
  • Author Response 27 Jun 2019
    Masato Oda, Independent Scientist, Japan
    27 Jun 2019
    Author Response
    1. Thank you for your precious suggestion! We changed the word "cultivation" to "plants" in the title. We think the word is more suitable to the content.
    2. Thank
    ... Continue reading
Views
43
Cite
Reviewer Report 09 May 2019
Azeem Tariq, UMR 951 Innovation SupAgro-INRA-CIRAD, Montpellier SupAgro-IRC, Montpellier, France 
Not Approved
VIEWS 43
The authors of "Rice cultivation reduces methane emissions in high-emitting paddies" present an effort in collecting and measuring the CH4 emissions, in three rice cropping cycles during the 100 days of the field experiment. The overall paper has been written ... Continue reading
CITE
CITE
HOW TO CITE THIS REPORT
Tariq A. Reviewer Report For: Rice plants reduce methane emissions in high-emitting paddies [version 2; peer review: 3 approved with reservations]. F1000Research 2019, 7:1349 (https://doi.org/10.5256/f1000research.17312.r39719)
NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article.
  • Author Response 22 May 2019
    Masato Oda, Independent Scientist, Japan
    22 May 2019
    Author Response
    Thank you very much for reviewing our manuscript and giving precious comments.

    I think your comments can be summarized to three points: “uniformity of conditions”, “the effect of early stage rice ... Continue reading
COMMENTS ON THIS REPORT
  • Author Response 22 May 2019
    Masato Oda, Independent Scientist, Japan
    22 May 2019
    Author Response
    Thank you very much for reviewing our manuscript and giving precious comments.

    I think your comments can be summarized to three points: “uniformity of conditions”, “the effect of early stage rice ... Continue reading

Comments on this article Comments (0)

Version 3
VERSION 3 PUBLISHED 29 Aug 2018
Comment
Alongside their report, reviewers assign a status to the article:
Approved - the paper is scientifically sound in its current form and only minor, if any, improvements are suggested
Approved with reservations - A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit.
Not approved - fundamental flaws in the paper seriously undermine the findings and conclusions
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