BG-2023-145_Forster_ response to RC2

Dear Referee 2.

Thank you for a thorough, critical and very constructive review. Your accurate analysis of wording and structure is particularly helpful (and impressive). It improves the message in this manuscript a lot and is much appreciated.

You understood what we did, the reasoning behind it and how we discussed our results correctly.  We understand your criticism and suggestions to improve the text, and therefore include most of your suggestions clarifying the text for the reader.

Our response below is indicated by “>” and follows the original comments by the reviewer, RC­2 (kept in bold).

General comments

With their study Forster et al. aim to qualitatively assess whether bottom trawling generates peaks in the sediment Chl.a profile that are similar to the characteristic subsurface concentration peaks that are commonly used as indicator of biological bioturbation. To answer their question, the authors conducted two experiments (one ex situ, one in situ) and in situ environmental sampling in the western Baltic Sea. With the results from the ex situ experiment mimicking trawling and the in situ experimental trawls the authors could show that peaks in the sediment Chl.a concentration profile are caused by re-deposition of Chl.a rich surface sediment through the otter boards (‘flipping sediment over’). The shape of these experimental Chl.a profile corresponds to the shape that is commonly associated with biological bioturbation and similar to the profiles detected in the sediment cores from random in situ sampling in an area that has both, bioturbating bivalves and intense bottom trawling. his highlights the question of physical or biological originality of those Chl.a peaks and the authors discuss implications and potential resolution of it. Because of the similar shape of Chl.a profiles from biological bioturbation and physical trawling in their study area, the authors put their findings into environmental context and present estimates of Chl.-a transport events from bioturbation and trawling. This discussion point is very interesting and I would have liked to read some more about their thoughts and arguments on the biogeochemical and ecological context of their findings.

> It is positive to see that the core of what we did and intend to present in this manuscript is understandable. You will find below that we have expanded the discussion on context and consequences of peaks and combined it with the issue that arises when the peaks’ genesis with respect to bioturbation or trawling is unclear.  

> following the first reviewer (RC_1) we altered some parts of the discussion already and, for instance, integrated Epstein et al. (2021) and other additional literature.

As we outline below, and following your suggestion we now restructure the discussion while keeping its general structure with three sub-headings.

The research question that the authors pose is realitively specific and ‘technical’ but it raises thoughts on the ecological significance of using tracers like sediment Chl.a concentration as tracer to quantify bioturbation of benthic macrofauna, especially in areas where trawling occurs. The conclusions that the authors draw are consistent with the evidence and arguments they present and they address the main question. However, I found that the main research question and the conclusions are not very clearly formulated in the main text and not easy to identify for the reader. The combination of ex situ and in situ experiments with environmental sampling build a strong realistic picture in the results though I could not fully grasp how the modelled results (Table 1) fitted into the story. Here I would suggest to provide some more description/explanation so that readers unfamilar with Soetaert et al’s models and Oberle et al’s scenarios can follow. I would also be interested if there exist publications of Chl.a profiles where the peak can clearly be attributed fauna bioturbation, or have shown those in experiments and whether those could be shown/re-drawn here for comparison if data available (e.g. from Morys et al. 2017)? Overall, the manuscript is written well, but a number typos exist and I personally found the sentence structure hard to read and sentences and paragraphs lacked connection and reading flow which it is hard to identify the meaning/relevancy as a reader.

Detailed notes

Title: maybe add ‘in marine sediments’ to end of title, so readers know which environment this is in/about?

> We include this suggestion. New title: Bottom fishery impact generates tracer peaks easily confused with bioturbation traces in marine sediments.

Abstract

Line 10: why introducing local and non-local transport in the abstract when not referring to it any further in the abstract? Instead I suggest to shortly introduce what is meant by tracer peaks as this is something unfamiliar readers might not know about.

> We omitted the second sentence here including the truly unnecessary differentiation between local and non-local. Instead, we inserted a new one: Bioturbation (particle reworking) includes downward transport of particles into the sediment as a major process and is sometimes detected as sub-surface maxima (peaks) of specific particulate substances (tracers).

Line 18: this sounds contradictory to me, as you just stated above that the peaks are not distinguishable. Please clarify what you mean here. I am assuming that when you put your findings into the environmental context of the study area then it becomes apparent that bioturbation is the dominating process generating the tracer peaks, at least in your study area.

> Correct.  To clarify this, we changed the last sentence in the abstract to: However, based on natural fauna abundance, behavioral information and fishery intensity data, we identify macrofauna and not otter boards as the dominant cause for peaks at the sites investigated here.

Introduction

Overall, I find that the Introduction is lacking flow (paragraphs not well linked) and a clear lead towards the research question and research aim of this study. I think the section would benefit from restructuring the paragraphs and identifying what is important to introduce to readers to understand the topic and what the knowledge gap/research question is. Some aspects currently provided in the Introduction might not be relevant, or at least the relevance is not clear, while some interesting aspects around the tracer peaks and trawling effects come short (especially at line 62).

Line 21-26: I suggest to add that bottom trawling affects ecosystem functions (Epstein et al. 2021)

> New sentence: Trawling affects ecosystem functions such as carbon storage (Epstein et al 2021) and sediment integrity (de Juan et al. 2015), and additionally interacts with other pressures on the benthic ecosystem such as contaminant deposits or hypoxia (Oberle et al., 2016b; Bunke et al., 2019; van Denderen et al., 2021).

Line 33-34: What kind of scenarios are presented by Oberle et al. (2016b)? I cannot see how the second paragraph about difficulties in detecting effects of fishing gear is linked to the research topic of this study. It might help to add a last sentence to that paragraph to show the connection to your research topic about tracer peaks.

> This paragraph was split in two. The first one addresses that sediments may also be disrupted by other processes than trawling: “Investigations aiming to detect and quantify the effects of fishing gear at the seafloor face the difficulty that patterns may also stem from disturbances, natural or anthropogenic, other than trawling (Bunke et al., 2019). …… “

> A new paragraph starting “Localization of the impact on the sea floor and … ” focusses on the problems associated with localizing precisely the trawling marks in order to then sample precisely  there, whatever is needed to assess the effects trawling has. “Measures such as swept area surface (SAR) of fishing intensity remain inaccurate in that they average bottom trawls over long periods (per year or per quarter) and relate the impact to comparatively large areas (several km²)”.

A final sentence has already been added in response to RC_1. “However, the damage to the surface sediment by otter boards may be local. Studies investigating the change of vertical distribution of sediment constituents demonstrate that an effect of trawling can be the removal of surface sediment and considerable alterations of matter concentrations and processes in this sediment surface layer (Mestdagh et al 2018; Morys et al., 2021; van de Velde et al. 2018). In an experimental dredge trawl Morys et al. (2021) found that sediment excavated to 2.5-3 cm depth piled up irregularly on the sides of the track.”

We are now more explicate as to why we introduce these problems.

Line 39: remove the ‘…’. 

> Done

Line 44: concentration profiles of what and where?

> The sentence has been changed to: “ … and creates peaks in vertical concentration profiles of particles in the sediment (e.g. chlorophyll used as a particle tracer).

Paragraph 4: Great that tracer distribution and peaks as sign of bioturbation are introduced and explained for less familiar readers. However, I could not quite follow from line 47-51 and how this is relevant. Also the end of the paragraph does not provide a concluding sentence about how this connects to the study focus.

> We have reduced the detail of information and separated the remaining information into separate sentences. This makes the issue of decay in tracer more understandable: “Peaks are observed regardless of the persistence of the tracers used, in stable tracers or tracers that decay or degrade with time. Natural decay of the tracer chlorophyll allows to “look back in time” for 100 - 150 days when its peak concentration has declined to 25 % of its original value. Decay thus determines whether a peak will remain visible or if the event merges into the overall mixing which is usually dealt with as diffusion analogue.” In the preceding sentence the terms stable and decaying replaced experimental and natural, respectively, therefore the line of thought should be clear now.

A concluding sentence states that “Chlorophyll as a particle tracer can therefore show relatively recent events of particle mixing only”, which is the introductory information needed here (natural, decaying tracer with about 1/3 of a year time frame looking back.

Line 56: ‘.’ after (Aller, 2014) ok and move sentence of ‘The western Baltic to next paragraph’ because this is a new topic unrelated to bioturbation and tracer peaks.

> Yes, the sentence is moved. Subsequent sentence changed to fit.

Line 59: chl-a  Chl-a (as you have introduced the abbreviation). This is the case several times in the manuscript, please correct and make consistent.

> Throughout the manuscript there will only be “Chl-a”

Line 61: Peaks of what?

> Now changed to “Chlorophyll peaks detected …

Line 62: ‘However, intense trawling raises the question of an alternative origin of the peaks.’ -> How so and where is the knowledge gap? Here the Introduction becomes interesting in my opinion.

> We agree that this point may need introduction. In conjunction with the next comment to paragraph 6 we moved the sentence towards the end of the introduction and after paragraph 6 (on Arctica), expanding the thought as a separate paragraph “under water video evidence.

“However, intense trawling raises the question of an alternative origin of the peaks. Previous studies (Oberle et al., 2016b), UW-video evidence, and a possible analogy to terrestrial soil turnover during ploughing triggered the idea of surface sediment subduction by otter boards. To our knowledge there is no evidence of this transport process in the literature.”

This also helps to explain how we developed the idea that sediments might be moved in this particular way in the first place.

Paragraph 6: how is this detailed description of A. islandica relevant to your research question?

> We shortened this paragraph by 4 lines removing information about depth, age and preferred sediment, thereby restricting the information to the Arcita to the minimum necessary in the context of bioturbation.

Line 71: 1999 benthic study -> reference missing

> done

Lines72: AFDM abbreviation without explanation (I know what it means, but I am not sure all readers know?)

> done

Materials and methods

Line 81-82: Combine sentences or switch them around, e.g. We investigated the changes of particle distribution brought about by the mechanic impact of otter trawling. For this, we performed experiments ex situ in a mesocosm mimicking trawl marks to understand the underlying mechanism and in situ by setting trawl marks to provide proof of principle of mechanisms. (Although this might be repetitive of the last paragraph of the introduction, or could be integrated there).

Line 88: make title ‘Ex situ experiment’

> done, and likewise for “In situ experiment” below

Line 93: change to ‘from the field site Schnaterman (SM, figure 1)…’ or similar, remove the ‘close by?’

> done

Line 96: is the Corg content relevant? If not, remove, if yes try and provide a value, maybe from previous publications?

> Removed, because irrelevant. This information on Corg is also removed from “In situ experiment”

Line 106: were controls placed before or after sediment manipulation? I could imagine that the sediment manipulation with the shovel and rake resuspended fine material that may have affected the surrounding surface area from where controls were taken?

> Controls were taken afterwards and this is now pointed out I the text. Since we did not see any resuspension effect, such as sedimentation of Chl-a on those controls, we will also point this out in the result section.

Figure 2: A and B not shown in the figure panels, only in the caption

> A and B are shown in the figures now, too.

Line 114: make title ‘In situ experiment’

> done

Line 119: Can you say anything about how sure you are that the untrawled area that you sampled hasn’t been trawled by other fisher boats previously? And if yes, how long before you ran the in situ experiment?

> Based on information by the federal fishery agency (Thünen Institute for Baltic Sea Research, Rostock) there was little activity in the study area. Our preceding geophysical acoustic survey showed few tracks compared to e.g. Fehmarn Belt.                

Admittedly, surveys of fisher boats in the Baltic are far from perfect. And geoacoustic information might also miss tracks. However, we know that tracks that are on the order of a few months old always show up clearly in acoustic images.               

For Chl-a as a tracer to work, our track needed to be fresh and we sampled this fresh material that was displaced. Older peaks from older tracks should have been documented in peaks with reduced Chl-concentrations due to the decay of chlorophyll with age. We cannot see any significant peaks in our individual profiles that would indicate an event producing a peak within the last 1-2 months (50% surface concentration) or 3-4 months old (25% surface concentration).

Thus we are certain that any possible previous trawling does not interfere with our interpretation of the relocation of fresh surface particle tracer, as shown in our Chl-a peaks.

Line 120: ‘Five 36 mm inner diameter cores were taken randomly in an area of 1 m² each.’ -> of the untrawled area or of the net area of the trawl or both?

> Each was meant to indicate that both areas were sampled; changed to make the information clear.

Line 134: each 10cm diameter slice was homogenized, right? Slices were not mixed together, I assume.

> Correct, now changed to homogenized

Line 144: What type of ethanol (quality, purity, manufacturer)?

> The information is now provided: > 96% denatured ethanol (WALTER-CMP)

Line 156: Were all models from Soetaert et al. used in your study?

> No they were not. Text now includes more information, also because RC1 asked for it: “Starting from model 3, all subsequent models include 'non-local' transport of tracer from the sediment surface to depth with increasingly complexity (injection, J, and ingestion, r).  There is no benefit in trying to differentiate between models of higher complexity (models 3, 4, 4a and 5), since fitting results seemingly differ owing to some horizontal heterogeneity in our data. Also, we lack observations that would allow differentiating mechanisms like particle injection in physical sediment turnover and comparing it to model results. Therefore, we grouped the fits of non-local models into a category “non-local” and do not interpret them further”.

Line 160: Why the grouping and no further interpretation? What is the aim for running this model in your study?

> The reason to run models is to arrive at a contrasting differentiation between non-local and local transport. This differentiation is qualitative, but arriving there in an objective procedure, by modelling, provides us with quantitative information on the transport intensity as well, which is not used in this manuscript. While this has been a bit confusing, it is now clear by our use of the term “qualitative” in the text in contexts of information that we provide.

The information now included (see answer to line 156 above) hopefully also clarifies this issue.

Line 161: remove the ‘&’

> done

Results

Line 166-174: What about the profiles of control, net and furrow from fig 4? They are not mentioned in the text at all but shown in the figure.

> This is true and we added to the description of results a little.

Figure 4: Why show shaded area when not relevant for the key results of your study? This raises questions as to what happened there exactly which distracts from your key result in my opinion.

> In order to avoid such discussion, we changed the grey field to not transparent and removed “elevated pigment levels generated by mishandling during preparation” from the figure heading. Removing all data that are not strictly relevant to the study would require truncating all eight tiles in this figure at 6 cm depth. This looks strange and raises the question if we really measured such shallow concentration profiles to any person active in the field. Therefore, we prefer to hide something without addressing it and only stating “Shaded areas in upper panels indicate pigment levels not relevant to the present discussion”. This hopefully keeps further question at a minimum.

We added ex situ and in situ in the figure to make this clearer and easily visible for the reader.

Line 193-201: Are these results (and Table 1) derived from modelling the data? To identify what type transport was present? So you did not use the model to quantify any transport rates? I think this part might need clarification.

> Yes, they are. We had to employ the model quantifying transport rates in order to arrive at the qualitative differentiation (through the model) between local and non-local. This information is now included in the first sentence: “We compiled the qualitative information on non-local versus local reworking retrieved from mixing.exe by giving the number of best fits in each category (Table 1).”

Line 195: put ‘net, mounds or furrows’ into brackets, remove the ‘-‘

> done

Table 1: Do I understand correctly that data from Fehmarn Belt are from your study but data from Mecklenburg Bay are from Morys et al.? This is not very clear in caption and table. Also, please clarify that the numbers in the tables depict numbers of profiles.

> You understood correctly, but this was truly not clear. We changed it accordingly.

Figures 4 and 5: Can you please provide figures with a bit higher resolution, so that they are easier to read and features come out more clearly?

Discussion

Overall, paragraphs are really short and not well connected lacking reading flow. Some paragraphs appear puzzled together with random statements that don’t seem connected or where the link to your study results is not apparent.

Subheadings: It would be great if the subheadings already present the key message of the discussion topics, makes it easier for the reader to orientate and grasp the story. I like the structure of the discussion in Uniqueness, Consequences, Ways to resolve, but the text in these sections does not really relate to the questions that you want to answer (Line 246-247).

> In conjunction with responses to Reviewer 1 and along the lines of your suggestions we have added substantially to several aspects of the discussion, such as which implications does the undefined origin of peaks have. We remove some distracting parts and rearrange (i.e. description of results into “results”) in order to streamline the reading flow. Keeping the general structure with “Uniqueness, Consequences, and Ways to resolve” has been a guideline though. Please find more details below.

Some final concluding thoughts at the end of the discussion would be great.

> These remarks had to be placed there, also following your last comment.

“Thus, we consider it conservatively safe to assume that the majority of peaks detected in Fehmarn Belt stem from A. islandica active on a daily scale. Bioturbation by A. islandica in Fehmarn Belt should thus be the more frequent particle reworking process when compared to otter board sediment reworking. Therefore, we may continue to interpret chlorophyll peaks as bioturbation traces in this area. The different mechanisms of sediment disturbance bear similarities such as the fresh organic matter injection below the sediment surface demonstrated here. We cannot elucidate with the present data the biological and biogeochemical effects associated, particularly the spatial magnitude of both mechanisms need better quantification for such a comparison. Future exclusion of fishery in the area will provide a test field in which the persistence of peaks may be tested and their origin confirmed. “

Line 211-247: I think a lot of this text belongs into the result sections or is repeated from result section and implications of the results are only partly touched upon. I suggest to shorten this text focusing on communicating your key results and conclusion from it and then continue with the following subsections (Uniqueness, Consequences, Ways to resolve) as these are your actual discussion.

> We removed all of the descriptive passages relating to peaks and concentrations in ex situ and in situ experiments (2 paragraphs) reducing this first part of the discussion to <60% of its original length. This content has been added to the results section in a shortened version.

Line 215: you mean biogenic?

> Yes.

Line 238: ‘cannot rule out…’ -> what implications does this have for your results? Please discuss.

> For the reasons given above (half-life of the Chl-a tracer, information on little previous activity, no visible peaks that could be interpreted given the background of decay time), we are certain that any possible previous trawling does not interfere with our interpretation of the relocation of fresh surface particle tracer, as shown in our Chl-a peaks.

Line 250-271 (Uniqueness): This sections has some interesting discussion points but I don’t see that the questions of whether ‘this problem is unique to our area of investigation in Fehmarn Belt’ is answered.

> I order to answer that question, we reduced the text to the following sequence of topics: (1) in the literature only decapping by trawling is described, (2) no publications on peaks generated directly from trawling, (3) thus we do not know of any comparisons like ours. (4) Indirect evidence for peaks from trawling comes from e.g. by Oberle et. al. (2016b) when, as in their case, tracer and trawling activity were locally tightly coupled AND peaks existed at a sediment depth exceeding that of bioturbation, but reached by large trawling boards. (In a way Oberle et al. (2016b) investigated an area with conditions allowing to draw conclusions based on different lines of evidence). Following this we state, as before, (5) that if peaks are at similar depth, as in our case, their origin remains indistinguishable.

“Uniqueness” now starts with “It is not clear if the problem of indistinguishable peaks exists in other fishing areas of the oceans, too.” It now ends with “We suspect that the origin of peaks in a given area can only be inferred if the bioturbating organisms, the gear used and intensity of fishing are known.”

“Line 255: you mean coarse? (found this typo more often, please check and correct)

> Yes we do. We corrected two such typos.

Line 267: ‘Boards and rolls keeping the net gear open.’ -> I don’t understand how this statement is relevant here? This is a good example of a seemingly random sentence, not connected to the content/topic of a paragraph, which happens a lot throughout the manuscript. Please work on the text structure/reading flow.

> We completely removed this passage.

Line 268: Are you talking about the furrow generated by the trawl here when referring to Morys and Bradshaw? And how is this linked to your results?

> We did, but this information is now incorporated in the discussion of uniqueness, addressing that in association with trawling, decapping has been directly observed (e.g. by those authors) but no peak generation.

Line 270-271: This has been said several times now.

> Now omitted.

Line 274-294 (Consequences): The authors touch on consequences of bottom trawling in this section, but I thought the question to be answered was what consequences/implications it has that bioturbation-induced peaks and trawl-induced peaks are not distinguishable? I think the latter would be a more suitable discussion topic linked to the research question and key finding of this study.

> We put a new line into this discussion, focusing first on the implications that each of the different ways that peaks may be generated have. Following this we discuss the consequences for our understanding and description of the ecosystem, if those peaks are not distinguishable.  In this context we retain some aspects of the geochemical/biological consequences that each of the process have (biological and physical peak generation), but we compare and contrast them subsequently.

“Implications/consequences” now starts with “The most notable consequence of indistinguishable peaks is likely that bioturbation studies may be suspected to overestimate the biogenic reworking effect.” We here note that “below (Ways to resolve) we will argue that this is not the case in Fehmarn Belt, however, this issue needs observation in other areas where trawling and bioturbation are prominent…” The massage now ends with “In conclusion, we argue that we need to know if peaks indicate trawling or bioturbation, because their effects on biota and the way they affect geochemical processes differ substantially. “

Line 275-280: This information from Oberle’s study needs to be given in the introduction where you refer to it for the first time and on which your study is based on or linked to (if I understood correctly). Then you can refer back to it here in the discussion.

> True, this is now used in “uniqueness” and introduced accordingly in the Introduction.

Line 296: Ways to resolve -> I read this section in the understanding that this refers to ways to resolve the issue that bioturbation effects and trawl effects can’t be distinguished in tracer profile, making their interpretation harder. I like this section and would suggest to elaborate a bit more on why it is important to resolve it and what aspects should be considered in which research contexts. For example, when quantifying and extrapolating bioturbation transport rates based on Chl.a profiles, your results imply that it should be checked whether there is frequent trawling in that area where the extrapolations are done and whether trawling might cause a bias in the bioturbation quantification. I feel, especially in this section, to add a focus on ecological and biogeochemical context (What does this mean?) might work well and shape the manuscript to fit better to the aims and scope of the journal.

> “ways to resolve” now starts with “In our Fehmarn Belt data set, we cannot assign a single peak with any certainty to biological or physical reworking. Can knowledge of the environment help to resolve this issue, since differences in peak generation likely indicate different effects in the ecosystem?”

It now ends with “Therefore, we may continue to interpret chlorophyll peaks as bioturbation traces in this area. “

Line 297-305: I do not see how this is related to resolving the issue.

> we omit this passage on half-life and step size. 

Line 307: This is the interesting question for this discussion section, but it needs to be made clear for the reader what the ‘issue’ is.

> The “issue” is now “that we cannot assign a single peak with any certainty to biological or physical reworking.

Line 313: 0.1 of what per quarter? Frequency or area?

> 0.1 per quarter implies that the area swept is 0.1 m² per m² in 3 months (quarter year). This information is given 6 lines later, but we include an explanation following “0.1 per quarter” as 10% probability for any area.

Line 319-320: Where did you get the probability assumption from or why do you assume this?

> This is related to 0.1 which is now explained as 10% probability

Line 333: So the numbers 480 vs 0.4 m-2 yr-1 reflect transport event per area and time? And what is your conclusion here, how can the issue be resolved?

> There is now an altered final sentence: “The numbers calculated suggest 3 orders of magnitude higher frequencies for biogenic non-local transport (480 versus 0.4 m^-2 yr^-1).”

And, yes, the result of this calculation (obtained for THIS area only) shows that peaks are predominantly of biological origin and therefore consequences discussed above are mostly related to bioturbation. And for Fehmarn Belt we may continue to interpret chlorophyll peaks as bioturbation traces.

 Literature included:

Epstein, G., J. J. Middelburg, J. P. Hawkins, C. R. Norris, and C. M. Roberts. 2022. The impact of mobile demersal fishing on carbon storage in seabed sediments. Glob Chang Biol 28: 2875–2894. doi:10.1111/gcb.16105

De Juan, S., Hewitt, J., Thrush, S., Freeman, D.: Standardising the assessment of Functional Integrity in benthic ecosystems. Journal of Sea Research 98, 33-41. https://doi.org/10.1016/j.seares.2014. 06.001, 2015.

Schiffers et al. (2011): omitted