Domestic Herbivores, the Crucial Trophic Level for Sustainable Agriculture: Avenues for Reconnecting Livestock to Cropping Systems

Round 1

Reviewer 1 Report

The opinion manuscript title "Domestic herbivores, the crucial trophic level for sustainable agriculture: Avenues for reconnecting livestock to cropping systems" suggests a breakthrough in approaches for increased agricultural productivity using environmentally sustainable practices.

A lengthy review of literature on past and present fertility management practices in various agro-systems is provided. However, the review is not organized in a logical sequence that clearly shows the anticipated crucial role of domesticated livestock in agricultural production or the alternative avenues for reconnecting.... The discussion needed to have been more on these two important items as highlighted in the tittle.

While the authors commented on the negative perception regarding the methane-related environmental impact of livestock systems, an important discussion on phophorus load from livestock systems that  pollutes surface water bodies is missing.

Although the stated objective of the opinion paper focuses on examining the past, present and future ecological roles of domesticated herbivores in agricultural productivity around the world, the actual discussion is only based on Europe-based systems and a brief mention of Brazil.

The acknowledge template needs to be populated or edited as relevant

Comments for author File: Comments.pdf

Author Response

Reviewer 1

The opinion manuscript title "Domestic herbivores, the crucial trophic level for sustainable agriculture: Avenues for reconnecting livestock to cropping systems" suggests a breakthrough in approaches for increased agricultural productivity using environmentally sustainable practices.

Responses to comments.

R#1.1. A lengthy review of literature on past and present fertility management practices in various agro-systems is provided. However, the review is not organized in a logical sequence that clearly shows the anticipated crucial role of domesticated livestock in agricultural production or the alternative avenues for reconnecting...

R#1.R1. This review section deals first with the historical role of domestic livestock in soil fertility, then the cause of disconnection of livestock and cropping system due to the use of synthetic fertilizers with the environment impacts is shown and explained, and finally in discussion we emphasize the necessity for re-coupling livestock and cropping systems. Because this logic in argumentation seems well followed and appreciated by the three other reviewers, we have not modified the sequence in the text, as suggested by R#1.     

R#1.2.The discussion needed to have been more on these two important items as highlighted in the tittle.

R#1.R2.Yes we have tried to focus more explicitly the discussion on these two points.

R#1.3. While the authors commented on the negative perception regarding the methane-related environmental impact of livestock systems, an important discussion on phophorus load from livestock systems that pollutes surface water bodies is missing.

R#1.R3. Yes Reviewer 1 is right: excess of P in environment has also a strong environment impact due to too high livestock stocking density…But this impact is not due intrinsically to herbivores, as for CH4 emission, but is due to the feed-lot system associated with the too high disconnection between livestock and cropping system. So we have developed a new paragraph on this problem (Lines 546-553) of too high P concentration and losses from intensified livestock specialized systems…. That should reinforce our conclusion in favor of integrated crop-livestock…

R#1.4. Although the stated objective of the opinion paper focuses on examining the past, present and future ecological roles of domesticated herbivores in agricultural productivity around the world, the actual discussion is only based on Europe-based systems and a brief mention of Brazil.

R#1.R4. We agree that this problem of reconnection between livestock and cropping system is also very crucial for Africa and Asia and we have added some discussions with relevant literature references (Lines 659-682).

R#1.5. The acknowledge template needs to be populated or edited as relevant OK

R#1.R5. Response to  remarks

“stigmatized”: I propose: “…are considered as being a problem because…”

All editing or English correction should be validated without problems….

“sustainability” in §3: I propose “the persistence of the soil fertility effect…”

R#1.6.  Comments in §4.1:

R#1.R6.  We would not follow the 3 remarks (p. 9) and I propose to answer as:

Lines 411-413. “Grasslands and forage crops are important components of herbivore livestock systems…. Animal itself, cannot be separated from its feeding system so that, differently from  monogastric livestock, herbivores are fully linked to grasslands and forage crops. “

R#1.7.  Comment on the end of § 4.2, just before Table 1,

R#1.R7. I propose to add: Lines 529-545. “This solution could help in substituting the use of N-P external fertilizers for cropping systems by (i) a more important contribution of N2 symbiotic fixation due to use of legume species as forage source; and (ii) the recycling of N-P in a more conservative way at local level. The great advantage of such a substitution from mineral N forms is that, N is provided with a high coupling with C, allowing a more direct use by soil microbes and then an activation of the MIT in soil as shown in the Figure 1. By this way, a two high NO3- and NH4+ accumulation in soil is avoided, reducing then the risk for N leaching and N2O emission as compared to situation where N fertilizer are applied under mineral forms. So it would be possible to maintain an overall agriculture productivity at local scale with reduced environmental footprint as compared to intensified and specialized systems. For achieving this recoupling between N and C, following the demonstration by Soussana and Lemaire 2014, it is necessary to avoid a too high stocking density in grazed grasslands because of excess of urine patches that does not allow rapid recoupling by MIT. For a more intensified system with higher stocking density at territory level, use of manure from barns correctly enriched with straw to reach a more uniform C/N ratio of about 10-15, should be the best way for providing N, P and other nutrients to crops without environment.

R#1.8.  Last comment:

R#1.R8. We agree with this remark. So we propose instead of “remains in opposition” to write “… is sometime not fully compatible with socio-economic and political constraints…”. But we think that the following sentences are very clear that despite great advantages of these integrated crop-livestock systems, there is a lot of options for changing the current system…. But this required more research out of the scope of our paper.

Reviewer 2 Report

The paper by Lemaire et al. provides an interesting comprehensive review/opinion about crop-livestock integrated systems. The work highlights the importance of these systems to build farm sustainability and, in my opinion, it is a useful addition to the body of literature on this subject. I think it has potential to be published in Agronomy after some improvements. Please, find my suggestions attached. 

Comments for author File: Comments.pdf

Author Response

Reviewer 2

R#2.1. The paper by Lemaire et al. provides an interesting comprehensive review/opinion about crop-livestock integrated systems. The work highlights the importance of these systems to build farm sustainability and, in my opinion, it is a useful addition to improve the body of literature on this subject. I think it has the potential to be published in Agronomy, after some improvements. I suggest the following revisions:

R#2.R1. Thank you very much for this positive comment. Here are our responses to your suggested improvements.

Abstract:

R#2.2. Please, synthesize and rewrite the abstract. The abstract is too long and does not provide a clear synthesis of your work. I suggest you clearly: introduce the topic of your work; list the main goals; and identify the main conclusions and future efforts/recommendations, including further research, as pointed out in section 5.

R#2.2.R2. R#2 is right. We have modified the abstract following your recommendations.

 Introduction:

R#2.3. First sentence: In plant nutrition potassium, calcium, and magnesium are macronutrients. In which scope are you referring to these nutrients? Please, be more clear.

R#2.3. R3. Thanks for your remark. K, Ca and Mg are important elements among the 35 elements necessary for plants, and they play an important role in soil fertility and in some situations they can be limiting for plant nutrition. We have added a sentence for explaining that (Lines 53-54).

R#2.4. The penultimate sentence of the first paragraph: Please consider changing “conversion of  agriculture to organic farming systems” to “conversion from conventional farming systems to  organic farming systems” if this was the case regarding the documents you are citing.

R#2.4.R4. We have done this change.

R#2.5. Last sentence of the first paragraph: Please, make sure this is the message of the paper you are citing (reference 12). The authors you are citing indeed concluded that “There is consensus that global transitioning towards a more plant-based diet is essential for maintaining planetary boundaries”. But they also conclude that greenhouse gas emissions resulting from  ovolac to vegetarian diets (which require livestock production) are ca. 35% lower than most current omnivore diets. This is a very controversial topic. Studies that do not consider the positive services of animals in agriculture can be identified by this flaw – which reinforces the message of your work. However, this flaw must be carefully pointed out and in line with the message of the cited colleagues, so that it is not easily questionable. I suggest you to confirm the meaning of the paper you are citing and rephrase the sentence if necessary. I also suggest you to 1) consider a new word instead of “banish”; 2) change “[they] forget” to “[they] did not consider” or a similar expression; and 3) change “methane emissions” to “greenhouse gas emissions” (the cited authors reported GHG in general – I suggest you to do the same, without specifying CH4).

R#2.5. R5. Yes we agree with this comment and we have changed this last sentence (lines 76-82) as follows :

“ There is consensus that global transitioning towards a more plant-based diet is essential for maintaining planetary boundaries (12). Nevertheless, some studies concluded on the need to reduce drastically herbivore livestock production because of their methane (CH4) emissions that is contradictory by the fact that greenhouse gas emissions resulting from ovo-lacto vegetarian diets (which require livestock production) are ca. 35% lower than most current omnivore diets (12). Therefore it is important to have a more global approach considering the essential role that domestic herbivores could play in agriculture sustainability through their ability to recycle and transfer mineral nutrients across agro-ecosystems to maintain long-term soil fertility (13).”

- Section 2:

R#2.6. End of the second paragraph: I suggest you to briefly introduce the herbivores' role here to link with the following information (internal and external cycling) – i.e., in this specific section 2 you mentioned “herbivores” for the first time in the legend of Figure 1 and not before that. I suggest you to make a clear link between the second and third paragraphs, highlighting the herbivores' role.

R#2.6. R6. Many thanks for this suggestion.  we have added this sentence (Lines 192-195):

“In these natural terrestrial ecosystems, large herbivores  species co-evolved with vegetation through their grazing and foraging activity leading to plant community perturbations associated to defoliation, and through their dejection leading to recycling of most of the nutrients of the mineralomass they have ingested.”

- Sections 3, 4, and 5:

R#2.7.  Sections 3 and 4 are both very interesting. Section 5 provides a good conclusion for this text. I have no specific suggestions.

R#2.7. R7. Thank you for your interest. 

- References:

R#2.8 Please make sure the references are according to the journal guidelines and confirm the DOI

(e.g., the DOI of reference 12 does not seem correct).

R#2.8. R8.  The reference list has been checked.

- All text:

R#2.9.  The ideas in the text are understandable, but in general sentences are too long (e.g., the first 2 sentences of the abstract have 5 to 6 lines). Please, proofread all of your text and - whenever possible - break long ideas into more than one sentence

R#2.9. R9. We fully agree and we have tried to shorten some too long sentences.

Reviewer 3 Report

Dear Authors,

the manuscript deals with an interesting topic: the role of herbivores in past and current agricultural systems. A clear point of view from the "rural" side against what is claimed from the "urban side" states the idea of the manuscript.  A good literature review is presented and the structure and lenguage guide the reader through a smooth lecture.

I have only minor suggestions that you can see in the attached file. Here a list with some general sugestions: i-check the way the words are split (there are some errors);  ii- chech number of tables and figures, there are some errors; iii- figures are difficult to read due to samall font size, it could be nice to enlarge figures particullarly Fig. 1, Fig. 6 (actually the manuscript says Fig. 3)  and Fig. 7 (now as Fig. 4).

Finally, it would be nice if you can provide an scheeme similar to the one presented in Figure 7 (actually Fig. 4) for French systems but for Brazilian - Campos conditions. If you do not have enough quantitative data, may be you can state it as an hypothesis and reinforce your last section of the manuscript. 

Comments for author File: Comments.pdf

Author Response

Reviewers 3

Dear Authors,

the manuscript deals with an interesting topic: the role of herbivores in past and current agricultural systems. A clear point of view from the "rural" side against what is claimed from the "urban side" states the idea of the manuscript.  A good literature review is presented and the structure and lenguage guide the reader through a smooth lecture.

We thank reviewer for this positive comment.

I have only minor suggestions that you can see in the attached file. Here a list with some general sugestions: i-check the way the words are split (there are some errors);  ii- chech number of tables and figures, there are some errors; iii- figures are difficult to read due to samall font size, it could be nice to enlarge figures particullarly Fig. 1, Fig. 6 (actually the manuscript says Fig. 3)  and Fig. 7 (now as Fig. 4).

Yes, please to excuse us for these wrong Figure numbering… We have corrected them and also tried to enlarge a little bit front size.

Finally, it would be nice if you can provide an scheeme similar to the one presented in Figure 7 (actually Fig. 4) for French systems but for Brazilian - Campos conditions. If you do not have enough quantitative data, may be you can state it as an hypothesis and reinforce your last section of the manuscript.

Yes, we agree with this suggestion but unfortunately the data we could use from these experiments in Brazil are not adapted for a similar interpretation because in these experiments we cannot have a comparison of each system managed at its optimum N fertilization…. But only a comparison of the 2 systems (grazed and ungrazed) managed with a similar N fertilization.

Responses to detail comments:

• Introduction: “reduction of food losses and food wastes”….? Yes we have added this point.
• Mention to “rice-fish system” Yes a sentence and a reference has been added
• “vaste from food industry” (reference added)
• Non-symbiotic fixation? Non-symbiotic N2 fixation has been well identified in section 2 as one of the source for N supply in soil in natural ecosystem. But here, the rate of non-symbiotic fixation remains very low in comparison to symbiotic N2 fixation through legume crop introduction within crop rotation and grasslands areas for being mention as a way for improving soil N…. So we have replace the “only” source by the “main” source
• “faster litter decomposition if C/N is too low….” The main effect here is the fact that N fertilization of pasture produced high N concentration of plants that accelerate mineralization of plant litter whatever the soil tillage management system. So we don’t think necessary here to discussed about an hypothetic effect of soil tillage here…
• “Biofertilizers”: in fact we wanted say “organic fertilizer”
•  

Reviewer 4 Report

The manuscript is well written, and while the ideas in it are not new, they are compiled in a comprehensive and convincing manner and have innovative aspects, such as the historical developments, thus making this manuscript nonetheless a useful review.

Given the high standard of the writing, only minor changes are required for publication. Most of the issues resolve around the figures or framing in the introduction and will subsequently be mentioned in detail.

Figures:

- In several figures, the font size of legends, axis etc should be increased. This is particularly true for Figure 1, Figure 3, Figure 4, 6 and 7.

- Figure 6 is called Figure 3 again in the figure caption, while Figure 7 is again called Figure 4.

- In Figure 7 (named figure 4 in caption, yet should be 7, page 14) the letters mentioned in the caption cannot be found in the graph. Furthermore, on the left side the three images are first title with Yonne, then Plateu de Borgogne (Yonne), and then Plateau de Borgogne. The right images are always linked to Orgeval, however in the caption, they are named Plateu de Borgeaugne and Brie (the latter being never mentioned anywhere in the Figure but presumably is Orgeval). Please make this uniform across all panels and the legend.

Table 1: I think a bit more explanation and discussion of the results would be interesting. The table could well be linked to the text before: what are the implications of these N flows, why are the relative N losses lower in mixed than in specialised systems.. This could be much more powerful to demonstrate the theoretical points that were made initially

Some of the statements use a valuing language and could be softened. I.e. on page 5, the CH4 emissions from ruminants are called an "ecosystem price", and on page 4 the CH4 emissions are called the "ecological way" to convert cellulose to human edible process. While I fully agree with the sentiment of the statements, they appear to be biased, given that the real and existing implications of the CH4 emissions for anthropogenic climate change are not mentioned anywhere in the text. Also, several issues that are highlighted later on in the text (particularly in the intensive feedlot systems having high N losses and feeding high amounts of cereal, thereby still having food-feed competition and not bringing any ecological benefits from the grasslands, as well as the need to have stocking densities that are adjusted for the potential of the land to take up nutrients), are neglected in the introduction, given the reader a false sense of "greenwashing" ruminant systems.

Finally, there are very small points regarding uniformity:

In text:

- Units are sometimes separated with a . (habitants.km-2) and sometimes with a / (habitants/km2; GgN/yr )

References: Please check uniformity. Sometimes DOI is written before the link, sometimes doi, sometimes just the link without abbreviation before, and this sometimes with http://doi.org/ and sometimes without. In reference 23 it also states dio in the link, instead of doi. In some References (e.g. 34, 38, 45,49,51,52....) the Journal title is abbreviated, whereas in others it is not

Author Response

Reviewer 4

R#4.1.The manuscript is well written, and while the ideas in it are not new, they are compiled in a comprehensive and convincing manner and have innovative aspects, such as the historical developments, thus making this manuscript nonetheless a useful review.

R#4. R1. Thanks for these positive comments.

R#4.2. Given the high standard of the writing, only minor changes are required for publication. Most of the issues resolve around the figures or framing in the introduction and will subsequently be mentioned in detail.

R#4.2. R2. Thank you, we will follow your recommendations.

Figures:

R#4.3.In several figures, the font size of legends, axis etc. should be increased. This is particularly true for Figure 1, Figure 3, Figure 4, 6 and 7.

R#4.3. R3. We fully agree and we have tried to make the legends and axis readable.

R#4.4 Figure 6 is called Figure 3 again in the figure caption, while Figure 7 is again called Figure 4.

R#4.4. R4. Yes we apologize for is error …. We have corrected it.

R#4.5 In Figure 7 (named figure 4 in caption, yet should be 7, page 14) the letters mentioned in the caption cannot be found in the graph. Furthermore, on the left side the three images are first title with Yonne, then Plateu de Borgogne (Yonne), and then Plateau de Borgogne. The right images are always linked to Orgeval, however in the caption, they are named Plateu de Borgeaugne and Brie (the latter being never mentioned anywhere in the Figure but presumably is Orgeval). Please make this uniform across all panels and the legend.

R#4.5. R5. We are very sorry. All these errors have been corrected

R#4.6. Table 1: I think a bit more explanation and discussion of the results would be interesting. The table could well be linked to the text before: what are the implications of these N flows, why are the relative N losses lower in mixed than in specialised systems. This could be much more powerful to demonstrate the theoretical points that were made initially

R#4.6. R6. We do not understand fully this comment. The sentence: “Thus, these systems use proportionally fewer resources than disconnected systems, but they produce a similar relative share of food for human nutrition and generate relatively less pollution” (Lines 497-499), shows clearly the advantage of integrated livestock cropping systems for reducing environmental impacts while maintaining food production? 

R#4.7. Some of the statements use a valuing language and could be softened. I.e. on page 5, the CH4 emissions from ruminants are called an "ecosystem price", and on page 4 the CH4 emissions are called the "ecological way" to convert cellulose to human edible process. While I fully agree with the sentiment of the statements, they appear to be biased, given that the real and existing implications of the CH4 emissions for anthropogenic climate change are not mentioned anywhere in the text. Also, several issues that are highlighted later on in the text (particularly in the intensive feedlot systems having high N losses and feeding high amounts of cereal, thereby still having food-feed competition and not bringing any ecological benefits from the grasslands, as well as the need to have stocking densities that are adjusted for the potential of the land to take up nutrients), are neglected in the introduction, given the reader a false sense of "greenwashing" ruminant systems.

R#4.7. R7. Yes we have tried to be more precise in discussion that the problem is not to  “maintain herbivore livestock as usual” but to reduced  local stocking densities where it is too high for the capacity of agro-ecosystem to recouple C-N and P (too intensive  and concentration of animal systems) and to re-increase these mixed systems where they have disappeared in order to have a well equilibrium between decoupling-recoupling processes. (see Lines 703-716).

Finally, there are very small points regarding uniformity:

In text:

R#4.8. Units are sometimes separated with a . (habitants.km-2) and sometimes with a / (habitants/km2; GgN/yr )

R#4.8. R8. The format of the units have been homogenized.

References:

R#4.9. Please check uniformity. Sometimes DOI is written before the link, sometimes doi, sometimes just the link without abbreviation before, and this sometimes with http://doi.org/ and sometimes without. In reference 23 it also states dio in the link, instead of doi. In some References (e.g. 34, 38, 45,49,51,52....) the Journal title is abbreviated, whereas in others it is not

R#4.9. R9. References have been checked and corrected.

Round 2

Reviewer 2 Report

As I wrote before, the paper is a useful contribution to improving the body of literature on integrated crop-livestock systems and emphasizing their importance in the current agricultural context. The authors have significantly improved the work and, in my opinion, it should be published in its current form.