Complex soil food web enhances the association between N mineralization and soybean yield – a model study from long-term application of a conservation tillage system in a black soil of Northeast China

Zhang, Shixiu; Chang, Liang; McLaughlin, Neil B.; Cui, Shuyan; Wu, Haitao; Wu, Donghui; Liang, Wenju; Liang, Aizhen

doi:https://doi.org/10.5194/soil-7-71-2021

Articles | Volume 7, issue 1

https://doi.org/10.5194/soil-7-71-2021

© Author(s) 2021. This work is distributed under
the Creative Commons Attribution 4.0 License.

https://doi.org/10.5194/soil-7-71-2021

© Author(s) 2021. This work is distributed under
the Creative Commons Attribution 4.0 License.

Articles | Volume 7, issue 1

Original research article

|

19 Mar 2021

Original research article |

| 19 Mar 2021

Complex soil food web enhances the association between N mineralization and soybean yield – a model study from long-term application of a conservation tillage system in a black soil of Northeast China

Shixiu Zhang, Liang Chang, Neil B. McLaughlin, Shuyan Cui, Haitao Wu, Donghui Wu, Wenju Liang, and Aizhen Liang

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Final revised paper (published on 19 Mar 2021)
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Preprint (discussion started on 10 Feb 2020)
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Interactive discussion

Status: closed

AC: Author comment | RC: Referee comment | SC: Short comment | EC: Editor comment

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RC1: 'Comments to the author', Anonymous Referee #1, 10 Mar 2020
- AC1: 'Response to RC1', Shixiu Zhang, 26 May 2020
RC2: 'English editing needed before peer review.', Anonymous Referee #2, 06 Apr 2020
- AC2: 'Response to RC2', Shixiu Zhang, 26 May 2020
RC3: 'Comments to the author and editor', Anonymous Referee #3, 07 Apr 2020
- AC3: 'Response to RC3', Shixiu Zhang, 26 May 2020
EC1: 'editor response to reviews', Elizabeth Bach, 14 Apr 2020
- AC4: 'Response to Chief Editor', Shixiu Zhang, 26 May 2020

Peer-review completion

AR: Author's response | RR: Referee report | ED: Editor decision

ED: Revision (15 Jun 2020) by Elizabeth Bach

AR by Shixiu Zhang on behalf of the Authors (16 Jul 2020) Author's response Manuscript

ED: Referee Nomination & Report Request started (14 Aug 2020) by Elizabeth Bach

RR by Anonymous Referee #4 (06 Sep 2020)

Suggestions for revision or reasons for rejection

Overview

This study examined how three tillage treatments (i.e., conventional till [CT], ridge till [RT], and no till [NT]) affected the relationship between soybean yield and the N mineralization of soil organisms. Using two soil depths, the investigators sampled N mineralization and the densities of soil organisms, including soil microbes (bacteria and fungi), nematodes, mites, and springtails. The authors found that food webs in RT and NT treatments released more N than the CT treatment, which appeared to correspond to higher crop yields in the RT and NT treatments. Although the energetic food web modeling is not new (see Moore and de Ruiter 2012 for details), the ecological context is novel and sheds insights into how the soil food web can contribute to N cycling and associated crop yield. It is also useful that the investigators directly measured N mineralization in addition to the energetic modeling; thus, the modeling can be loosely compared to N mineralization rates for each treatment. The manuscript is generally easy to follow, and the replication and methodological approaches appear appropriate.

While the manuscript covers an important topic in soil and agroecology, the presentation of the analyses and results were not as effective, so the study’s novelty and impact are less apparent. More detailed comments, which I hope the authors find helpful, are below.

Concerns

I think the manuscript can benefit from a discussion (either in the Introduction or Methods) on the utility and limitations of energetic food web modeling. Indeed, these methods have been used for several decades now, but they are not mainstream, and many readers interested in this study will likely be less familiar. From my understanding, energetic food webs are highly parameterized theoretical models that are meant to give crude estimates of C and N cycling rates through food webs; the results are not meant to be interpreted as absolute. Addressing these expectations/limitations upfront should help eliminate the confusion of why so many parameter values are derived from different systems while also elucidating the usefulness of this method.

Furthermore, there should be a figure that illustrates the energetic food web models (similar to Figure S1), ideally showing all three tillage treatments so that they can be compared visually (see Pressler et al. 2018 for example). The line size of each pathway should indicate the strength of the interaction between food web compartments (the ‘igraph’ package in R is one way to do this). I would also suggest eliminating (or reducing) Table 3 that shows the same information or placing that information in the appendix.

I propose adding a separate section for the Sensitivity Analysis under the ‘Statistical Analysis’ heading in the Methods. Explicitly state what was done and if the results are consistent when using different feeding preferences and/or different food web configurations (see Koltz et al. 2018 for example) -- simply stating that “a sensitivity analysis was performed by re-assigning omnivorous collembolans into fungivores and herbivores (50% each)” is not sufficient. A formal sensitivity analysis would help evaluate the robustness of the results in this ecological context. There should be text explaining how it was performed in the Methods, reported in the Results, and discussed in the Discussion.

The various types of tillage treatments need to be clearly defined in both the Introduction and Methods section. What is the difference between conservation tillage vs. conventional tillage? Which one of the experiment treatments is considered to be conservation tillage? Is the NT the control treatment? There appears to be a disconnect between the terminology used in the Introduction and Methods; the terms should be consistent and clear throughout the manuscript. Not all readers will be familiar with agricultural practices.

The hypotheses in the last paragraph of the Introduction need to be developed further. Why do you expect there to be more N release from conservation tillage from conventional tillage? Why would soil depth be pertinent for determining the influence of soil organisms regarding N mineralization?

Overall, the Discussion is long and disorganized. I suggest starting with a short summary of the results, making sure to highlight the key new insights, followed by a discussion of if the hypotheses were supported or not. The middle paragraphs should be used to explain what the findings mean within a broader context, drawing on support (or contrasting support) from the literature. I will reserve the section on study limitations and commentary on the sensitivity analyses for the section right before the Conclusions paragraph.

Other comments

The Abstract is confusing. I’m not sure what results are from the energetic modeling, N mineralization measurements, or other associated analyses. For example, in Lines 46-48, is this the energetic modeling result, or is this from the biomass estimates of the trophic guilds? In general, the Abstract needs to be summarized more effectively, as the current take-home message is unclear.

The way the experiment is described is somewhat misleading, as at first read it appears that the experiment and its sampling have been going on since 2001, which was not the case. To make the experimental design clearer, I suggest stating the time interval of the tillage treatments (e.g., 2001 – 2015) and mention that this study only sampled for N mineralization and soil organisms in 2015.

The extraction of 120 hours at room temperature is not standard for Berlese-Tullgren funnel methods. What is the justification here, and how do you know that all arthropods were extracted if there wasn’t a heat gradient?

Although there is information on the various groups of soil fauna sampled in Table S1, it would have useful to include the average densities and standard errors for each taxonomic unit according to tillage treatment. Soil core extractions will usually capture springtails, mites, and nematodes – which of these groups and functional guilds were most abundant?

The assumptions of the model are acceptable and similar to previously published models (e.g., Schwarz et al. 2017, Koltz et al. 2018, Pressler et al. 2018). However, because some of the literature values are from very different regions and study systems, the authors should explain why these parameter values are appropriate for this study. Obviously, it would’ve been nice to measure and confirm each parameter value, but that is usually impossible to accomplish for these types of models.

Lines 221-223: I would recommend stating if the N mineralization equations are modified from de Ruiter et al. (1993), and if so, how?

Lines 305-314: The Results don’t do an adequate job in covering how the food web modeling relates to the crop yield. Maybe I missed this, but is there a way to loosely compare the energetic food web modeling to the crop yield data?

References

Koltz, A. M., A. Asmus, L. Gough, Y. Pressler, and J. C. Moore. 2018. The detritus-based microbial-invertebrate food web contributes disproportionately to carbon and nitrogen cycling in the Arctic. Polar Biology 41:1531–1545.

Moore, J. C., and P. C. de Ruiter. 2012. Energetic food webs: an analysis of real and model ecosystems. Oxford University Press, Oxford, UK.

Pressler, Y., E. J. Foster, J. C. Moore, and M. F. Cotrufo. 2017. Coupled biochar amendment and limited irrigation strategies do not affect a degraded soil food web in a maize agroecosystem, compared to the native grassland. Gcb Bioenergy 9:1344–1355.

De Ruiter, P. C., J. A. Van Veen, J. C. Moore, L. Brussaard, and H. W. Hunt. 1993. Calculation of nitrogen mineralization in soil food webs. Plant and Soil 157:263–273.

Schwarz, B., A. D. Barnes, M. P. Thakur, U. Brose, M. Ciobanu, P. B. Reich, R. L. Rich, B. Rosenbaum, A. Stefanski, and N. Eisenhauer. 2017. Warming alters energetic structure and function but not resilience of soil food webs. Nature climate change 7:895–900.

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RR by Anonymous Referee #2 (22 Sep 2020)

Suggestions for revision or reasons for rejection

Overall comments: One year of data is simply not enough to draw the conclusions you have done here. This is a long-term study so why not include historical yield data? There were no crop yield differences and the mineral N concentrations, in 0-15 cm depth, were contrary to expectations. The estimations for N cycling within the soil food web are therefore rendered difficult to interpret or meaningless. If only one year of data is presented, without any data on growing conditions, could it not be simply that N mineralization was controlled more by soil water content and temperature?

Ln 6, replace "Relationships" with "Relations", and remove "of soil organisms"

Use "relation" throughout, where applicable.

Ln 7, as it stands, the title is rather broad. I would suggest making it more specific. For example, you could include where the study was conducted as part of the title.

Ln 33, suggest changing "promoting" to "to promote"

Ln 34, again, in the N being mineralized exclusively from soil organisms themselves? You could say "by soil organisms", or just "...N mineralization and soybean ..." because the process is assumed to be biologically driven/mediated.

Ln 41, as you plowed to 20 cm but only measured the N release to 15 cm you cannot say "thoughout the plow layer". Rephrase.

Ln 44, it is unclear what a "plant channel" is and how it mineralizes N.

Ln 42-46, the logic of this sentence is hard to follow. It is also a run-on sentence. Soybean yield was related to N mineralization, though fungal, plant, and bacterial channels (?) and this somehow demonstrates the role of spatial variability? Remove "demonstrating the role of spatial variability of soil organisms in linking N mineralization to plant growth".

Ln 47, the sentence would need to define what "energy channel" you are referring to. Be specific.

Ln 51, change "optimal" to "maximum". Optimal is a subjective term and you have not defined it here.

Ln 60, include citation(s) that state this.

Ln 61-63, you have omitted portions of the soil N cycle. Simply because N recovery in plants from fertilizer application is not 100% doesn't mean that all is lost. Immobilization could be a factor as well. Or that pools of inorganic N in soil build up. So, include all possible loss pathways in your statement.

Ln 63-66: How does one exploit the role of soil organisms? Make your meaning explicit.

Ln 73: In what form is the excreted N? Is it plant available?

Ln 79: What accounts for the rest of the N mineralized? Don't leave the reader wondering here.

Ln 80-82: I think that this statement is too bold. It would seem that your citation refers to the second part of the sentence, i.e., conservation tillage can promote richness and abundance of soil organisms. You need to cite the source of your statement that conservation tillage is "one of the most effiicent practices to maintain optimal productivity". Presumably you mean agricultural practices. In what way would it be efficient? No-till systems can take several years to "settle", so chemical fertilizers are likely more efficient in that sense. Also, what is "optimal"? Maximum?

Ln 97, please clarify what you mean by "benefit". Who or what benefits here? The producer? But in what sense?

Ln 99, what changes are you referring to? Be specific and start the sentence with the subject.

Ln 102-104: I would expect mention of soybean from the title of the manuscript. In the title you say "soybean yield", so is it just one crop or all?

Ln 108, specify the time frame? Over a rotation? Over the entire length of the study? Season? Or from week to week?

Ln 109, I think that you should be precise about what the "key role" is that you are looking at. How will you judge if a set of organisms plays a "key role" at one depth and not at another?

Ln 119: Missing article at the beginning of this sentence.

Ln 124: Please choose one system of spelling and be consistent. Here you mix British and American.

Ln 126: Could you please state what the common practice would be in the study area? How common is seeding maize and soybean into ridges?

Ln 124-128, since tillage systems are the focus of your research you should refer to the specific instruments that were used. Make and model. As you would for analytical equipment. This is needed to judge the relative intensities of the systems. The reader likely won't know what a "modified lister and scrubber" looks like or who intense the soil modifications would be.

Ln128- 132, Please provide an explanation as to why residues were replaced. Is this meant to mimic the amount of residue left in such systems under commercial circumstances? Are you not biasing the results by not incorporating the residues in the CT? The lack of inputs in the plough layer would presumably have an influence on the soil biology.

Ln 135-136, please provide all relevant information on experimental design here so the reader doesn't have to refer to a separate article. This information is important to the current work.

Ln 137, specify what years the data were taken in.

Ln 152, you should also include weather and climate data. How representative of the historical precedent were the times when you measured?

Ln 149-152, specify in what years you measured crop yield.

Ln 217-219, provide a justification as to why the assumption of equilibrium is valid. If C:N shifts, SOM buildings or decreases then it would seem that this assumption is not valid?

Ln 246, stating it in this way would seem to say that you transformed the data prior to testing for assumptions. This would be an incorrect approach.

Ln 255, please explain what you mean by "channel".

Ln 265-266, please properly cite all R packages used.

Ln 270-275, please specify the form of N that you are refering to. nitrate, ammoniumn, or total?

Ln 271, This statement would appear to incorrect according to Table 1. RT > CT but NT is not different than either, at 0-5 cm.

Ln 272, it is probably not appropriate to call the 5-15 cm depth the "deep layer" as you have measured N content at an even deeper layer.

Ln 273, this trend is not significant, so in fact, your analysis shows that CT > RT = NT.

Ln 323, a description of how this was done should be in the Materials and Methods section.

Ln 367-369, Rephrase this statement, it is misleading. CT>NT, but RT was not different than either.

Ln 369-370, Again, it is misleading to insinuate there were differences when in fact, Table 1 states that there were no signficant differences in crop yield.

Ln 451, it would be more appropriate to say that "we estimate" since you did not measure this directly.

Ln 456, never were the mineral nitrate concentrations higher in NT than CT, nor was crop yield higher in NT than CT, so this statement is misleading. Please re-phrase.

Table 1, when were these soil samples taken? At the end of the season? If there were no yield differences, in one year at least, but there was a difference in mineral N left after harvest (?).

Ln 635, please remind the reader where these data came from.

Ln 637, please rephrase without using repetitive terminology.

Referee Report: PDF

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ED: Reconsider after major revisions (05 Oct 2020) by Elizabeth Bach

AR by Shixiu Zhang on behalf of the Authors (13 Nov 2020) Author's response Manuscript

ED: Referee Nomination & Report Request started (24 Nov 2020) by Elizabeth Bach

RR by Anonymous Referee #4 (03 Dec 2020)

Suggestions for revision or reasons for rejection

I am pleased with how the authors addressed my initial concerns. The novelty and ecological importance of this study are much clearer in the revised manuscript, particularly with the additional background on the energetic modeling, sensitivity analyses, and associated figures comparing the different tillage treatments. Their explanation of the experimental design, sampling protocols, and statistical analyses is satisfactory. This study should make a valuable contribution to our understanding of how conservation tillage practices can influence soil food web energetics.

I do have several suggestions that should be incorporated into the revised manuscript to improve clarity and eliminate typos/errors:
Line 31: Change to “achieve a new equilibrium in the soil environment”
Lines 33-34: Change to “in such a situation” ... “how the soil community regulates nutrient cycling impacting crop growth is not well documented”
Lines 36-37: Delete “continuous application”
Line 39: Delete “pool”
Line 40: Change to “plant growth will vary”
Lines 44-45: Change to “using energetic food web modeling.”
Line 47: Change to “A similar trend…”
Line 56: Should be “potential mineralizable N pool”
Lines 56-57: ”which is a cornerstone for conservation tillage system to achieve the sustainable crop productivity” – This sentence fragment needs revising; I’m not sure what you mean here.
Line 87: Should be “potential mineralizable N pool”
Line 95: Change to “when the soil environment”
Line 97: Change to “situations”
Line 105-107: This sentence needs to be revised; hard to understand
Line 123: Change to “plant growth will vary”
Line 161: Change to “prevent water and wind erosion”
Line 179-182: I think instead the authors should acknowledge the limitations of data collected in only one year.
Line 193: Need to close out the sentence with a closing bracket
Line 206: Change to “The microbial community”
Line 232-234: The arthropods are not extracted at room temperate if there is a heat gradient from the lights. I would delete the phrase “at room temperature” because it is confusing and not the standard language for describing this method.
Line 526: Should be “potential mineralizable N pool”

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ED: Revision (11 Dec 2020) by Elizabeth Bach

Dear Zhang et al,
Thank you for your revision of the manuscript “Relations between mineralized N delivered by soil food web and soybean yield after long-term application of conservation tillage system in a black soil of Northeast China” submitted to SOIL. I agree with reviewer 4 that the manuscript has improved greatly. There are a few lingering concerns from the previous round of reviews that must be addressed if the manuscript is to be published:
• Must address caveats pertaining to 1 year of data
• Must clearly present as a modeling study that sets-up hypotheses for future studies to test, not as empirical data. The final sentence of the conclusion (lines 530-535) does this, but it needs to be evident in the abstract, the results, and early in the discussion.
• There is lingering confusion about the relationship of these results to soybean yield. The title and paper clearly tie the soil food web modeling to soybean yield, yet in response to reviewer 2, it is stated “Our study was focused on investigating how the whole soil organism communities regulate nutrient cycle impacting crop growth not on the variation in crop yield among different tillage practices.” There is a subtle difference in soil community contribution to crop growth vs. tillage differences in crop yield. Crop growth was not measured in this study, yield was, and the paper repeatedly ties the results back to soy yield and tillage practice.

In addition to these, reviewer 4 has provided some minor revisions. I would be willing to consider a revision of this manuscript that addresses these concerns.

Please let me know if you have any questions or concerns.

Sincerely,
Elizabeth Bach
Topical Editor, SOIL
elizabeth.bach@tnc.org

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AR by Shixiu Zhang on behalf of the Authors (14 Jan 2021) Author's response Manuscript

ED: Publish subject to technical corrections (25 Jan 2021) by Elizabeth Bach

ED: Publish as is (08 Feb 2021) by Johan Six (Executive editor)

AR by Shixiu Zhang on behalf of the Authors (13 Feb 2021)

Short summary

Long-term conservation tillage results in more complex and heterogeneous activities of soil organisms relative to conventional tillage. This study used an energetic food web modelling approach to calculate the mineralized N delivered by the whole soil community assemblages and highlighted the essential role of soil food web complexity in coupling N mineralization and soybean yield after a 14-year application of conservation tillage in a black soil of Northeast China.