PSTR-D-21-00005

Maximising sustainable nutrient production from coupled fisheries-aquaculture systems

PLOS Sustainability and Transformation

Dear Dr. Willer,

Thank you for submitting your manuscript to PLOS Sustainability and Transformation. After careful consideration, we feel that it has merit but does not fully meet PLOS Sustainability and Transformation’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

This is an very comprehensive study highlighting the importance of limiting production of major fed aquaculture species such as salmon that mainly depend on the wild-caught fish meals and fish oil (FMFO). This study provides three alternative production scenarios in order to improve sustainable production of nutritious seafood based on Scotland’s farmed salmon industry.

Overall the paper would require some Major Revision before it is reconsidered for publication. Beyond the comments of the two Reviewers please consider the comments of the Section Editor provided below.

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We look forward to receiving your revised manuscript.

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Alexandros Gasparatos

Section Editor

PLOS Sustainability and Transformation

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Additional Editor Comments (if provided):

This is an very comprehensive study highlighting the importance of limiting production of major fed aquaculture species such as salmon that mainly depend on the wild-caught fish meals and fish oil (FMFO). This study provides three alternative production scenarios in order to improve sustainable production of nutritious seafood based on Scotland’s farmed salmon industry.

Overall the paper would require some Major Revision before it is reconsidered for publication. Beyond the comments of the two Reviewers please consider the comments of the Section Editor provided below.

Section Editor comments

The Introduction lacks the description of current knowledge/evidence on how reduction of major fed aquaculture species (e.g., salmon) production or other approaches regarding optimizing aquaculture and wild fisheries production could influence (positive and negative effects) sustainable nutrient production, sustainability in the marine environment, and fisheries-aquaculture systems. This can help the authors make a clear statement of how their study represents an advance on current knowledge. I do not ask a comprehensive review but some better framing of the study as the Introduction is rather basic at this stage.

In the Methods please a description of the study system (e.g., the salmon industry in Scotland). Again this should not be an exhaustive review but contain some important aspects to understand the study system.

Please justify why choosing the three alternative production scenarios somewhere at the beginning of Section 4.3. Please also consider developing a figure to represent visually the study scenario with all their basic elements. Would be really helpful for easy reference, as by the time the reader reaches Discussion many of the aspects of the scenarios have been forgotten due to the density of the provided information.

The Results and Discussion are well-organized. The discussion reveals the advantages and disadvantages of three scenarios for Scotland’s farmed salmon industry, and shows a nice application on a global scale. However, what is the limitation of this work and the feasibility of the scenarios? The former can be added in a new short sub-section at the end of the Discussion. The latter can be added also these, or in the individual sub-sections. Maybe consider using a table if it makes it easier.

Please provide the Conclusions as a stand-alone section. The length and content is generally fine, but maybe try to have some small content on future outlook.

Please create a single supplementary material in pdf or word that contains all the tables. Please make sure that all these tables are cited in the main text. It looks like it now, but please double-check. Also after each reference please add something (Table S1, Supplementary Material) to further help the reader.

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. Does this manuscript meet PLOS Sustainability and Transformation’s publication criteria? Is the manuscript technically sound, and do the data support the conclusions? The manuscript must describe methodologically and ethically rigorous research with conclusions that are appropriately drawn based on the data presented.

Reviewer #1: Yes

Reviewer #2: Yes

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2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: N/A

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3. Have the authors made all data underlying the findings in their manuscript fully available (please refer to the Data Availability Statement at the start of the manuscript PDF file)?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception. The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

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4. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS Sustainability and Transformation does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

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5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: Willer et al Maximising sustainable nutrient production from coupled aquaculture-fisheries systems

This study uses a scenario based analysis of how to best optimise the use of aquatic resources for human consumption by illustrating the seafood quantity and nutritional implications of diverting forage fish species to either feed aquaculture products or for direct human consumption. The authors explore 4 scenarios using Scottish Salmon as a case study. Looking at scenarios where a given supply of seafood (normalized to a serving size of 140g in this case) is sourced from 100% scottish farmed salmon (bau), scottish salmon (fed fish oil by trimmings only) and the european portion of forage fish that were previously used in feed complemented by a fraction of tropical forage fish species previously used as feed (II), scottish salmon (fed fish oil by trimmings only), mussels and the same fraction of tropical forage fish species previously used as feed (III) or scottish salmon (fed fish oil by trimmings only), carp and the same fraction of tropical forage fish species previously used as feed (IV). In each case they analyse the total seafood produced, wild fish biomass spared relative to the bau scenario and the nutritional outcomes (across nine micronutrients) for the portion sized unit of seafood supply.

The authors also apply scenario II to a global scale, limiting the supply of fish oil to salmon production to allow a greater expansion of species only marginally reliant on forage fish ingredients and increase the amount of wild fish available for human consumption.

Overall, I enjoyed reading this paper. It is well thought out, written and executed. And the nutrient outcomes are quite stark. I would support its publication. I think a few things need to be clarified throughout the paper beforehand though:

These scenarios aren’t really consumption scenarios, they are supply scenarios with the supply normalized to a portion size. I found the use of consumption throughout a bit confusing.

Greater reflection on the trade-offs of not using forage fish in feeds. The authors discuss the challenges of getting people to eat mussels or carp instead of salmon which I appreciated but I think the scale of this challenge is somewhat understated. Wholesale changes in diets are extremely hard and with huge numbers of people expected to come into a global ‘middle-class’ in the next few years, this affluence change is expected to drive huge shifts in demand for luxury products such as salmon, lobster, tuna etc and create considerable production incentives for lucrative export oriented products. At present this challenge is partially dealt with but insufficiently in my opinion. Another point is that pond aquaculture is often cited as this far more beneficial form of aquaculture (which is true in many ways) but it is by no means benign and has its own challenges which often remain unaddressed, especially under climate change. Some discussion of this is needed

Some reflection on that a 140g seafood portion will not be homogeneously divided by the proportions indicated here. Some people will get access to more salmon, others mussels, other more carp and others wild fish, so inequity will still exist under these scenarios in terms of the distribution of nutritional benefits.

Additionally, salmon aquaculture not using these fish does not necessarily leave them in the sea. Policies imposed to restrict salmon aquaculture and promote carp farming could initially lower fishmeal and oil prices that subsequently drive incentives for greater fishmeal and oil inclusion in animals that are not traditionally carnivorous because of the growth benefits inclusion could create. Not to mention how agriculture could respond. Only effective fisheries management and enforcement will mean they stay in the water. Greater elaboration on this point is needed. See relevant discussions by Anna Farmery on underutilized fish https://onlinelibrary.wiley.com/doi/abs/10.1111/faf.12467 and Ben Halpern on the efficacy on cell-based seafood introductions https://onlinelibrary.wiley.com/doi/abs/10.1111/faf.12541

I have made some specific comments below

INTRODUCTION

Line 58 - A little pedantic but aquaculture does and will continue to make up a very small proportion of global food supply. Suggest stipulating aquatic food demands/ animal-source food demands or something to that effect

Line 63 - this is a little broad brush given that aquaculture is incredibly diverse and the sustainability of any system inescapably depends on context. What is a sustainable food system given all are under strain from a human population growing in affluence and number? Agriculture, crops and livestock, and dependence on capture fisheries are all unsustainable in a number of contexts that they take place so this is more a feature of food systems in general. Of note is that the aquaculture sector is highly motivated to improve sustainability and the improvements to date have been quite incredible, particularly around feed sourcing - the topic of this paper. I think what is clear is that aquaculture provides an opportunity to make sure that if we are to meet demand for animal source food we must do so as efficiently and equitably as we can. As the aquaculture sector is growing very quickly but still young and a focus of much innovation it provides an opportunity to really improve production practices.

L 66-67 -0- it absolutely could, but to note is that it is not just because aquaculture is using it that it isn't consumed more directly. That conversation is more complex and nuanced than aquaculture ‘taking it’.

Line 67 - 68 - more general but related is that aquaculture not using forage fish for feed will not automatically leave them in the ocean.

Line 74-75 - think this is the wrong reference. The paper by Bjorn Kok references a paper by David Little who in turn references his other paper with Richard Newton https://link.springer.com/article/10.1007/s11367-017-1386-8 which should be the right one re this statistic. For Scottish salmon at least. There is also the one by Nathan Pelletier et al for a more global picture https://pubs.acs.org/doi/10.1021/es9010114.

METHODS

L 390 - suggest putting the sources of the data before the reference for reader information.

L 443 - I find the use of diet scenarios a confusing term - is this feed diets or human diets? I’m guessing the latter given no Atlantic Salmon have a diet of 100% Atlantic Salmon in terms of business as usual. But it should be clarified - they are really supply scenarios, that would be a far clearer way to phrase it.

L 455 - again who is consuming the wild caught fish - people or farmed fish? So scenario 2 diverts forage fish from European EEZs previously used for feed towards human consumption? Consider rephrasing to be clear.

L 464 - this data can be presented on aggregate for a global level though right? Gets at a probabilistic estimate without digging into trade data - might not be a bad supplementary plot.

L 474 - this is unclear - what does leaving all other species unused mean? They remain as feed fish, they are used for neither feed nor food, or they are only used for human consumption? Think you need to be very explicit in what you are doing in each scenario. A table of the scenarios and what you are doing clearly demonstrated would help.

L512-514 - are these the production volumes of the end users or that of the FMFO for each end user? Pretty sure you mean the former but needs clarification.

Carp and mussels - substitutability, landscape impacts of carp, evenness of supply i.e. some eat carp, some eat salmon - who decides? Price?

L 543 - Does halving the fishmeal allocation mean production stays stable? Because feasibly you could also double the production with the same fishmeal allocation too? Thus increasing the efficiency of conversion….

RESULTS

Figure 1c - is the catch on the x axis - actual fishmeal and oil biomass? If so I suggest you label it as ‘Catch in combined fishmeal and oil equivalents (t)’ or something to that effect to absolutely clarify.

Figure 2b - also clarify what the error bars mean here. I’m assuming the uncertainty derived from the minimum and maximum contributions to fishmeal and oil among species?

Line 139 - clarify what you mean by local. To my understanding, this is fish from European EEZs? I think many would raise eyebrows to southern Europe being ‘local’ to Scotland.

Line 141 - what do you mean by ‘spare’ - in the ocean?

L 141-144 - I would avoid statements of ‘this amount of fish is eaten’ - you don’t model consumption here, just edible quantities. So I would suggest something more along the lines of “For a given unit supply in edible portion equivalents….this much is available from wild fish and this much from farmed salmon’.

Figure 3 c - what does the spare wild-caught fish mean? Is this the wild forage fish spared from use? In which case they would not be ‘caught’. Suggest clarifying through different phrasing.

DISCUSSION

L187-189 - this is an unlikely scenario given that the industry is already responding to supply shortages and price increases, and zero fishmeal and fish oil formulations for salmon are already in circulation. Many fish sparing (meal and oil feeds) are now commercially available, Veramaris seem to be leading the charge on this globally https://www.veramaris.com/press-releases-detail/veramaris-wins-f3-fish-oil-challenge.html. To me, what you study does is maintain a plausible level of fish oil delivery to salmon and it remains static in this case (which is totally fine). But with new feeds coming into the fold this could still allow salmon to grow without an increasing wild-fish footprint.

L200 onwards re effectiveness of new feeds - also consider Cottrell et al 2020 Global adoption of novel aquaculture feeds https://www.nature.com/articles/s43016-020-0078-x

L 221 -235 also once forage fish is not used for aquaculture, the response in price may make in attractive to agriculture once more. Which aquaculture has largely displaced.

L 275 - interesting! Although would the inclusion of Schizochytrium in microcapsules increase the energy (and at present the GHG) footprint of mussels? My understanding is that manufacturing and maintaining these SCPs is still quite energy intensive?

L 299 - yes not to mention the general landscape effects of increasingly intensified carp production. Trade-offs abound here.

L307 - this paper by Belton et al, while very eloquent, omits the considerable challenges facing land and freshwater availability under climate change for the expansion of carp farming or the disease constraints from continued intensification.

L307 Challenges - these are considerable challenges.Reversing consumption trends is not easily done.

L 310 - curious to know the relative health effects of processing carp products in this way.

L335 Perhaps fairly easy with California having a somewhat negligible aquaculture industry, where there is considerable industrial pressure to do so, this may not be so straightforward.

Reviewer #2: I have added my review with attached file. It is considered to be a quality and useful study or modeling.

The article can be accepted if necessary corrections and arrangements are made in accordance with the recommendations given.

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Reviewer #1: No

Reviewer #2: No

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Attachments

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Submitted filename: OYILDIRIM REVIEWING-Maximising sustainable nutrient production from coupled fisheries.docx

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Submitted filename: QUALITY FISH MEAL.pdf

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Submitted filename: Aquafeed Industry in Turkey.pdf

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Submitted filename: A Cursory Look at the Fishmea.pdf

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Submitted filename: Production_of_Fish_Feed_and_Fish_Oil_from_Waste_Bi.pdf

Maximising sustainable nutrient production from coupled fisheries-aquaculture systems

PSTR-D-21-00005R1

Dear Dr.

We're pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements. 

Within one week, you'll receive an e-mail detailing the required amendments. When these have been addressed, you'll receive a formal acceptance letter and your manuscript will be scheduled for publication. The journal will begin publishing content in early 2022.

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Kind regards,

Semra Benzer, Prof.Dr.

Academic Editor

PLOS Sustainability and Transformation

Additional Editor Comments (optional):

The above manuscript, entitled "Maximising sustainable nutrient production from coupled fisheries-aquaculture systems" with David F Willer as contact author has been submitted to PLOS Sustainability and Transformation.

It is appropriate to accept the publication in line with the corrections made and the referee's recommendation.

Best regards

Prof.Dr. Semra BENZER

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #2: All comments have been addressed

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2. Does this manuscript meet PLOS Sustainability and Transformation’s publication criteria? Is the manuscript technically sound, and do the data support the conclusions? The manuscript must describe methodologically and ethically rigorous research with conclusions that are appropriately drawn based on the data presented.

Reviewer #2: Yes

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3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #2: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available (please refer to the Data Availability Statement at the start of the manuscript PDF file)?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception. The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #2: Yes

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5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS Sustainability and Transformation does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #2: Yes

**********

6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #2: The article appears to be suitable for publication.

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7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

Do you want your identity to be public for this peer review? If you choose “no”, your identity will remain anonymous but your review may still be made public.

For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #2: Yes: Önder YILDIRIM

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