Review of “Reviews and syntheses: Review of proxies for low-oxygen

paleoceanographic reconstructions”

by

Babette A. A. Hoogakker et al.

Summary:

Hoogakker and colleagues provide a very extensive review of various proxy approaches (ranging from trace elements & their isotopes, over biomarkers, nitrogen isotopes, and foraminifera-based proxies) that can be used to reconstruct marine oxygen changes over the Cenozoic. The amount of information included in the paper is immense and has almost textbook dimensions (100 pages of text, including 16 figures, and >53 pages of references). In my opinion, this can be seen as a strength and a weakness of the paper – and I suppose it is an editorial decision if Biogeosciences wants to publish such an extended review study or if it would be better to split the review paper into multiple review studies to make it more manageable for readers and also reviewers (a lot of different subsections have a separate introduction already).

Given the paper's extensive nature, I will concentrate my (more detailed) comments on the initial sections, up to and including Section 6.2.6.3. I will provide more general comments, particularly on what I perceive as the manuscript's primary limitation - its structure.

Overall, I am convinced that the information provided by the manuscript will be of great value to the community, but, in my opinion, the text should be shortened significantly. I initially thought the manuscript would be a fantastic way to learn about different proxy approaches used to quantify paleo-oxygenation changes, but I got discouraged by the very long text and vast amount of subsections of the manuscript. This might be fine for general readers who can pick and choose the sections they are interested in (in contrast to a job of a reviewer). However, I still think that a more focused text and a better organization of subsections would improve the usefulness and approachability of the manuscript.

General comments:

Comment #1.1: Shortening the manuscript and combining duplicate information

Considering the long list of authors and diverse topics covered, I suppose that different groups of authors were responsible for different sections – which is absolutely fine and necessary – however, the manuscript would benefit from a few core authors reviewing the entire manuscript and combining/deleting overlapping information (as also suggested in the review by Ellen Thomas; with nitrogen-dynamics being discussed in multiple sections only being one example).

Comment #1.2:

At times, the manuscript is quite wordy and/or provides a lot of detail on topics that are not directly related to the understanding of the specific redox proxies. A few example parts (mainly of the first half of the manuscript that I looked at in more detail) that could (in my opinion) be shortened are: Sections 3; 6.1.1. (especially in 2^nd and 3^rd paragraph); 6.1.2.

Is the information of the “Materials/Methods” type sections really important for the review paper (e.g., 6.2.2, 6.3.7, 6.5.3, 6.6.4, 6.7.3)? I found these sections rather technical and not very informative/crucial for understanding the specific proxy (but that might, of course, be personal preference).

Some of the future directions sections are rather long (especially 6.2.6 & 6.6.8 & 6.7.8).

The introduction to “6.5 Foraminifera trace elements” (6.5.1+6.5.2) consists of more than 7 pages (just text) plus 4 Figures. It should be possible to shorten this text (or combine figures) without losing too much relevant content.

Comment #2: Structure

The manuscript includes too many subsections (sometimes up to 5 levels—see, e.g., Subsection in 6.2.3), which is confusing and makes it challenging to pinpoint where the current information ‘lives’ in relation to the overall structure of the manuscript. I think a depth of 3 or 4 subsections should be enough; otherwise, the reader loses orientation.

Section 6 consists of many, many subsections and forms the majority of the text. In contrast, the previous Sections 1 – 5 are very short and do not have any subsections. This should be better balanced. For instance, why are Sections 4 and 5 separate Sections at all – this information could be part of the general introduction. Section 6 could maybe be organized into multiple Sections of similar size (potentially just the current subsections of Sec. 6).

Comment #3: Introduction

The introduction does not introduce the topic of the review article. The second paragraph explains the causes for ocean deoxygenation and the second half of the introduction exclusively deals with problems in Earth system models to simulate ocean oxygen correctly. This is very surprising as Earth system models are not part of the review paper at all.

More relevant would be a general introduction to oxygenation changes over the Cenozoic and redox-proxies, and how they can help quantify the oxygenation changes. Information given in the different intros throughout the document could here be combined(e.g. such as the information given in 6.1, 6.2.1 and similar sections throughout the manuscript).

Comment #4:

6.2. “Sedimentary redox trace elements and isotopes”

An overview table would be very useful that summarizes/compares the key characteristics, residence times and applications of the different proxies.

Also, for Subsections 6.2.3: Why not combine the elements & their isotopes in one section?

Comment #5:

The large amount of references for some sentences (sometimes 6-12) makes it difficult to read the text (just a few examples: lines 261, 521, 561, 575, Sections 6.2.3.1.4, 6.2.5.2 in general, 628, … ). It would be helpful to shorten the references given, e.g., only provide the most important references are given or a few examples. Also, it is not necessary to cite the same paper multiple times in consecutive sentences (for instance, see 6.2.3.1.2; 6.2.3.1.4; 6.2.3.3.1)

More Technical Comments:

First two sentences of Section 2: Please rephrase. It sounds like seawater temperature, pH, and dissolved oxygen are environmental properties that can generally not be measured directly.

Fig 1: the caption says: “Proxy types shown in olive

can be used to reconstruct oxygen from benthic settings, those in green can be used for pelagic settings.” But I do not see olive and green proxies in the figure.

Ln 389: “Fully digested” what does this mean – not clear for a non-data person.

ln. 547: decomposition of organic matter is probably meant here. Organic carbon describes only the C itself contained in organic material. Please check the use of organic carbon throughout the document.

Some of the subsection titles are rather long and should be shortened, see e.g. Subsections 6.3.3; 6.3.6

Title 6.6.3 = 6.6.2 -- I suppose, 6.6.3 is Planktic foraminifera

Line 398: “This is especially true ...” please rephrase, it is unclear what 2 to 3 cm kyr-1 referes to.

Fig. 4: It could be made more obvious what boundary condition is changed between a and b.

the relatively low-oxygen concentration at a certain depth below the seafloor (blue line) leads to aU precipitation (green line).

Line 709: … the occurrences of (singular)

Figure 8: Please include the figure in higher resolution. In particular, the text looks pixelated.

Comments on Hoogakker et al. Reviews and syntheses: Review of proxies for low-oxygen paleoceanographic reconstructions.

This is a comprehensive review that covers all aspects of proxies for oxygen deficiency as well as a broader suite of related biogeochemical processes. Given current interest in marine deoxygenation, it is certainly timely and will be widely read by the extensive research community working on oxygen proxies. The structure of the review is quite complex, with a lot of sections and subsections, and would benefit from some reorganisation. I have made specific suggestions below, as well as some editorial suggestions and comments directly on the pdf.

Suggestions for improving structure

1)  The Introduction mainly deals with the state of oxygen in modern oceans, drivers of deoxygenation and the difficulties of modelling current and future oxygen concentrations. The final paragraph of the Introduction (lines 119-143) stands out because it  discusses in some detail, and at some length, the difficulties of representing oxygen in models of ocean physics. This may be important background information, but it gives the impression that it is what the review is about. The actual topic of the review is referred to only in the final sentence, where it appears almost as an afterthought (‘We also need proxy-based oxygen reconstructions….’).

The rationale for the review, and its structure, are only outlined later in sections 4 and 5. I would suggest some editing of lines 119-143 to make this paragraph a bit shorter and less detailed and then following it with the justification for the review and its format, currently given in sections 4 and 5 (on p. 8). The section on proxies (currently section 2) would then follow on logically from this introduction.   

2)  Section 3, Figure 1. You introduce the term ‘Oxygen Deficient Zone’ (with capitals) for the first time in Fig. 1, whereas oxygen minimum zones (without capitals) are first mentioned in the Introduction; subsequently, the terms are referred in the text as ODZs (54 times) and OMZs (25 times), so together they figure quite prominently in the text. Fig. 1 shows the ranges of oxygen concentrations that each of these two kinds of zone is associated with, which would imply they are different. However, it’s never explained what the terms mean and what, if any, are the differences between them. You often seem to use ODZ as a synonym of OMZ (e.g., p.46-54). Section 3 would be the obvious place to clarify whether these terms refer to different things, or whether OMZs are a particular kind of ODZ.  

Perhaps you could also mention in Section 3 the different units used to measure oxygen levels and maybe also the conversion factors for switching between them. In this case, the section heading could be simplified to 'Terminology and units'. You seem to use µmol kg^-1 consistently, except in a few places where other units creep in. These include nM in line 1527; µmol/L on Fig. 10 axis (p. 62); µmol on axis of Fig. 13 (p. 70).  

3)  p. 21 and 22 - Section 6.2.4 (Organic carbon and trace element burial) and Section 6.2.5 (Other factors controlling trace element metal preservation/metal isotope fractionation). Perhaps I’m misunderstanding, but given the title of section 6.2.5, I’m unclear why these two sections are given equal status. If you rename 6.2.5 ‘Factors controlling trace metal preservation and metal isotope fractionation’ (i.e., delete ‘Other’), then you could renumber this section as 6.2.4 and place the existing Section 6.2.4 as a subsection of it (6.2.4.1), along with those current numbered 6.2.5.1-6.2.5.5.  

4)  Section 6.6. This whole section seems overly complicated and quite confusing. The short introduction (6.6.1) mentions only benthic taxa, whereas section 6.6 covers planktic taxa as well. The following subsections 6.6.2 to 6.6.6.2 switch twice from benthic to planktic with two sections on methods in between. I would suggest putting everything relating to benthic forams together under one heading (split into two subsections), followed by a section on planktic forams. So the arrangement would be something like this -

6.6. Foraminiferal assemblages         

Under this main heading you could add one or two sentences (not a separate section) to introduce the topic.

6.6.1. Benthic foraminifera

6.6.1.1. Relationship to bottom-water oxygen and proxies (your ‘Historical perspectives….’ Section).

6.6.1.2. Factors influencing proxies and their interpretation. This would include your current section 6.6.6.1, which includes two biological topics: the interplay between oxygen and the organic matter supply, and nitrate respiration.  

 6.6.2. Planktic foraminifera

6.6.2.1. Relationship to water-column oxygen. Perhaps this could combine your sections 6.6.3 and 6.6.6.2 since there only seems to be a tenuous distinction between them.

I’m not sure what to suggest for your sections 6.6.4 and 6.6.5 (which I think could be combined) and your section 6.6.7 (Marine archives and limitations). Are these just about benthic species or about both benthic and planktic species? If the former, then I would put them after the benthic part.  If the latter I would put them after the planktic part.    

Section 6.6.8. is also problematic. First, the remarks about the importance of images (lines 2105-2112), which come under this main heading, could be merged with lines 1995-2001 (section 6.6.5), with which they largely overlap. Second, I don’t believe that 6.6.8.1 and 6.6.8.2 are sufficiently different to merit separate subsections. If lines 2105-2112 disappear, then you could combine 6.6.8.1 and 6.6.8.2 as section 6.6.8 with the title ‘Future directions and open questions.

Section 6.6.9 Contribution to Morphological Proxies. I’m not convinced that this belongs in the section on foraminiferal assemblages as proxies. It reads more like an introduction to the next main section on foraminiferal morphometrics (6.7). I suggest you combine it with Section 6.7.1. It also overlaps to some extent with section 6.7.2.2.

Other points

Are the first three words of the title a statement of the manuscript type?  If not, then I suggest shortening it, e,g. – ‘Proxies for low-oxygen paleoceanographic reconstructions: reviews and syntheses’.

1. 9. Section 6.1.1. I’m not sure that the statement - ‘The presence of laminations is a key indicator of conditions that are inconsistent with the survival of benthic fauna beyond seasonal timescales’ (line 255-256) is necessarily correct. Microbioturbation that is not visible to the naked eye has been described from laminated sediments in the Santa Barbara Basin (e.g., Pike et al., 2001 Geology, 29, 923– 926). This presumably reflects the presence of meiofaunal organisms such as nematodes and forams, which can survive on very little oxygen (or in the case of forams no oxygen).
2. 10. Please specify here whether you are referring to low resolution CT scanning or high resolution micro-CT (µCT) scanning.

Line 623 etc. The Carter et al. (2020) paper doesn’t seem to be included in the reference list.

1. 34, Line 1006. You define BHP in line 1002, but you don’t explain anywhere what BHT means, as far as I can see.
2. 70, Fig. 13 caption says that the figure compares 4 oxygen indices, in each case based on the main species and the complete assemblages. Data for different indices are shown in different colours and the legend indicates two shades of each colour, one for main species, the other for complete assemblages. However, the figure includes only four lines of data (green, yellow, blue, pink), one for each index, with no differentiation between main species and complete assemblages.
3. 71. Section 6.6.4. Analyses and required resources. You refer to ‘wet or dry sieving to separate different size fractions’. It would be useful to say a bit more about the use of different size fractions (usually  63, 125, or 150 µm, sometimes 32 or 250 µm) because these have a strong influence on the composition of foraminiferal assemblages and so are an important issue when analysing them.  
4. 72, 6.6.6. Section heading. Here and elsewhere, I’m not sure that ‘Proxy drivers’ is the best expression. It doesn’t sound quite right. Perhaps ‘Environmental influences (or ‘controls’) on proxies’ would be better.
5. 72, Lines 2004-2004. Some metazoans can survive at very low oxygen concentrations. For example, high density, although low diversity, assemblages of nematodes flourish at 0.05 ml.L‑1 off Costa Rica (Neira et al., 2018, Frontiers in Marine Science). A polychaete species is dominant at oxygen levels of 5-6 uM on in the Pakistan margin OMZ (e.g., Jeffreys et al. 2012, Marine Ecology Progress Series).

Lines 2044-2045. I’m not an expert in this, but from what I understand, the storage of nitrate allows them to live in the absence of nitrate as well as oxygen. So having stored the nitrate, they can migrate to even deeper sediment levels where there is even less competition and danger of predation. When the nitrate stored in vacuoles is exhausted, they move back up into the nitrate zone and refuel.  

Line 2090. I’m not sure what you mean by complete foraminiferal assemblages. For modern faunas, this term would refer to the live plus dead assemblage. Obviously, that can’t apply to fossil assemblages. Perhaps you could call them ‘mixed assemblages’

Lines 2116-2118. You could mention that foraminiferal populations can fluctuate over inter-annual, as well as intra-annular time scales, even in the deep sea. Also, it would be worth adding a few words to touch on the wider issue of  temporal and spatial heterogeneity and the need to analyse replicate samples in order to provide a realistic assessment of the species-level composition of modern assemblages.

6.6.8.2. Lines 2140-2145. There’s also ancient DNA, which can reveal ecosystem changes over historical and longer time scales across a wide range of taxa. I think this will become an increasingly important tool.  For example -

-  Barrenechea Angeles et al. (2023). Encapsulated in sediments: eDNA deciphers the

 ecosystem history of one of the most polluted European marine sites. Environment

 International,172, 107738. https://doi.org/10.1016/j.envint.2023.107738.

-  Pawlowska et al. (2022). Ancient foraminiferal DNA: A new paleoceanographic proxy. https://doi.org/10.5194/egusphere-egu22-9392 EGU General Assembly 2022

Table 2, pp. 79-81 occupies a lot of space. You could reduce the size by 1) deleting the left-hand column (‘Foraminifera’), and 2) inserting an extra row at the beginning of the benthic entries, merging the cells into one cell stretching across the width of the table, and putting BENTHIC in bold centred in the middle of this cell. The other column headings would remain above this merged cell. The same could be done above the planktic entries. 3) You could then make the three right-hand columns wider, so that the entries in the cells take up less vertical space.

Line 2373-2376. ‘Nevertheless…..’. Is the intention here to contrast Bolivina pacifica with B. spissa?  In this case, it would be better to start the sentence with ‘On the other hand….’

 Minor grammatical issues

I’ve made editorial suggestions directly on the pdf, which I hope will improve the clarity of the text. 

In places, paragraph breaks are only indicated by a carriage return. Please indicate them by leaving a blank line, as you do elsewhere in the text.

Please hyphenate ‘bottom water’ when used as an adjective (bottom-water oxygenation’)

‘Foraminifera’ is a noun. Please write ‘foraminiferal’ when using the taxon name as an adjective - e.g. ‘foraminiferal species’, ‘foraminiferal assemblages’ (not ‘foraminifera species’ etc). You could also use the phrase ‘assemblages of foraminifera’.