Benthic Foraminiferal Indices and Environmental Quality Assessment of Transitional Waters: A Review of Current Challenges and Future Research Perspectives

Round 1

Reviewer 1 Report

The manuscript of O’Brien and co-authors is well written and reads quite easily. It definitely has the potential to become a valuable contribution to the special issue of the journal “Water”, entitled “Ecological Quality Status Assessment of Aquatic Systems: New Methods and Perspectives for the Future ».

In view of the title, I would expected that the manuscript of O’Brien and co-authors would present a review of benthic foraminiferal indices in transitional waters, and would identify current challenges and future research perspectives.

In my opinion, in this first version, these aims are only partly achieved. The manuscript presents a long introduction explaining the need and utility of foraminiferal bioindication methods (Chapters 1-2). The paper then continues with a presentation of the methods which have been developed until now (chapters 3-4) and a short fifth chapter (5) in which the foraminiferal indices are compared between themselves and with other indices. A sixth chapter describes then the recent advances in molecular studies. Further perspectives are presented in a very short eighth chapter.

Although the present manuscript is a good start, I think that to produce a valuable and useful publication, a major revision is necessary. My overall impression is that for the moment, the paper does not present enough new ideas to be of great utility.

The first four chapters basically repeat information that is easily available elsewhere, without much synthetic efforts. Consequently, this more or less obligatary part of the manuscript does not add very much to the existing literature. This chapter systematically mixes information for transitional waters (TW’s) and open marine systems, and is not exhaustive when it comes to presenting previous studies. I think that this chapter would have have been much more useful, if, after a short general introduction, if would have focussed exclusively on TW’s, and would have given an exhaustive overview (at least as supplementary material) of all foraminiferal biomonitoring studies that have been performed in TW’s. Evidently, it would be very useful to give a definition of TW’s at the beginning.

Chapter 5 presents a short (non exhaustive) text in which several foraminiferal indices are compared between them, or with biotic indices based on other organisms. Also here, this chapter would gain in strength if it would have been limited to TW’s alone.

The 6^th chapter, on molecular studies, is at present clearly the most useful part of the manuscript, what is explained by the very rapid evolution of this research field during the last years, so that a text reviewing the present status of this research field is not available yet.

Chapter 8, which presents the remaining scientific questions and research perspectives, is very short and rather general. In my opinion, this chapter should be the most important one of this review paper, by presenting some well thought, clear and precise (and possible new) guidelines for future research. I would like to incite the authors to make an effort to considerably improve this important chapter, by presenting a much more precise list of remaining scientific questions and targets, and by outlining the strategies to be applied to answer these questions and to achieve these targets.

In a large majority of examples presented in the manuscript, these examples are taken from studies in which the 3^rd author has been personally involved. In a review paper I would expect a more equilibrated presentation of the research efforts of the whole community.

Finally, I would say that the general tone of the manuscript tends to be overpositive. At too many places, it is stated that this or that method works very well, without giving convincing arguments to corroborate the authors’ opinion. I think that the authors should pay particular attention to this point, because the credibility of their manuscript heavily depends on it.

More detailed remarks:

The abstract makes it insufficiently clear what is new in this manuscript. Even in an overview paper like this one, I would expect some new ideas and/or eye openers.

The mix of information concerning open marine and transitional waters bothers me throughout the manuscript. I think that it is far from evident that methods applied in open marine ecosystems do also work in TW’s. I think therefore, that the information should be rigorously separated, and that emphasis of this paper should systematically be on TW’s.

I am surprised that there is not a short discussion on the use of living versus total (living + dead) assemblages, since much/most of the older studies in transitional waters have used total assemblages.

The introduction of chapter 6 and chapter 6.1, on eDNA, essentially deal with the same topic! There doesn’t seem to be a good reason to have a separate chapter on eDNA. 

On lines 733 to 735, it should be better explained why eDNA is considered as complementary, and can not be used as a stand-alone technique! This means that the disadvantages of the eDNA method have to be better explained!

In the chapter on perspectives, which is at present extremely general, I read (line 796) “There is now a need to constrain the biotic response of different foraminifera species to naturally stressed environments like transitional waters, to propose robust foraminiferal indices….”. However, from the running text, I got the strong impression that the biotic response of foraminifera to naturally stressed TW environments is well known, and that robust foraminiferal indices exist since quite some time already. This sentence seems therefore to completely contradict the general sense of this review paper.

Many more detailed remarks can be found in the annotated version of the manuscript.

Comments for author File: Comments.pdf

Author Response

The authors of the manuscript would like to thank each reviewer for their constructive comments, which have certainly helped to improve the quality of the overall document. 

Responses to the reviewer’s comments are in italics and please see the attachment. 

Author Response File: Author Response.pdf

Reviewer 2 Report

The paper presents an overview of bio-monitoring indices based on benthic foraminifera, which are applied to assess ecological quality status of marine habitats. Transitional waters, such as estuaries or the intertidal zone, have natural sources of environmental stress (e.g. highly variable salinity or high organic matter flux), and the use of biotic indices have not been very successful. Benthic foraminifera are a relatively new tool of bio-monitoring. This overview of possibilities offered by the foraminiferal tool to assess the quality of transitional marine habitats is timely and relevant. 

 

I recommend moderate to major revisions.

 

General comments

 

1. ‘Transitional waters’ are announced in the title. The Introduction defines transitional environments and clearly demonstrates the challenges of biotic indexing in these settings. The rest of the paper leaves this venue of ‘transitional waters’ and discusses studies from all epicontinental habitats including even coral reefs; the scope of the paper becomes fuzzy. I think the paper would have had evident outcomes if the authors concentrated on transitional waters. If the authors prefer to speak of foraminiferal indexing in all habitats, they should explain what is new as compared to earlier reviews. Then the title and aim should be changed accordingly.

 

2. The paper describes foraminiferal diversity indices and foraminiferal sensitivity indices (section 4). What is missing is a conclusion, indices of which type are more reliable in transitional environments. The same question applies to the fossil record. Do the authors conclude that sensitivity indices are reliable in transitional settings, or diversity indices, or both?

 

3. The Introduction shows that it is problematic to delineate natural stress and anthropogenic stress in transitional habitats (line 63). I cannot find a corresponding conclusion. Do foraminiferal indices help to resolve the issue?

 

4. My general impression is that the text is rather a narrative of published research, which can be shortened in places (e.g. paragraph 510 ff). From the other hand, I feel the authors do not say much what they conclude and predict. Characteristically, the Abstract lacks conclusions the authors have drawn. I believe the paper will become more attractive if the authors say in the Abstract which specific indices they conclude reliable in which transitional habitats.

 

5. The studies cited in Section 4.2 deals with all different types of marine habitats. Please restrict the selection of study areas to transitional waters (as the title of the paper claims) or explain how the text of this section applies to transitional habitats.

 

6. Speaking of molecular methods (section 6), the authors mention only the bright side. What is the auditorium of this paper? If the paper addresses decision makers, and the authors advocate the molecular approach, then the review in its present form is fine. If the auditorium is researchers, the review, I think, should be more balanced. Consider mentioning complications of metabarcoding, for example: many OTUs have not been identified to the species or genus level; the complex nature of foraminiferal nuclear genome poses the issue of several haplotypes of the barcode sequence present in one specimen; due to unpredictable amplification and other sources of noise the number of reads does not correlate to the abundance of specimens (the morphological assemblage and the metabarcode assemblage are hardly comparable); indexing based on foraminiferal metabarcoding needs calibration for the fauna from each geographic region.

 

7. I like the logics of the paper, but in a few cases I completely disagree with the logical link. I very much doubt that “retaining of smaller species,” if we keep in mind that the knowledge of their ecological preferences is next to zero, “improve the overall accuracy of palaeoenvironmental reconstructions” (line 719).

 

8. Another statement that leaves me in much doubt is in line 729. The authors cite papers that characterize the degradation of ancient DNA in marine sediments due to oxidation of organic matter and conclude “that obtaining genetic data is possible from oxygen depleted systems, like transitional waters which… can often be naturally enriched or anthropogenically polluted with organic matter.” If there is a relevant study, refer to it explicitly. If this is just an assumption, do not make it sound like a solid fact. Under anoxic conditions, organic matter decomposes with other electron acceptors, such as nitrate or sulfate, and DNA may decay as rapidly.

 

Specific comments

 

9. This is a review paper, and this is said in the heading. However, the title and Abstract are the only things people see in aggregators, and I suggest the review nature of the article should be explicitly indicated either in the title or in Abstract.

 

10. The structure of the review set by 1st level heading is logical, but there are elements that may need attention. Section 4 is devoted to indices based on foraminifera. Strangely, section 2 (paragraph line 153ff) also presents briefly this information. My impression is that this paragraph falls out of the logic flow. Please consider rearranging. I would omit this paragraph from section 2 and would retain all information on foraminiferal indices to section 4.

 

11. The aim is missing at the end of the Introduction (line 104) and is placed at the end of section 2. It is not obvious to me what is behind this unexpected placement. Consider moving the aim to the Introduction. If not, perhaps it will help if the Introduction says where the aim will be presented. The way the aim is formulated (paragraph 178-181), it does not include transitional waters, which are announced in the title (though it is said in the following paragraph). I strongly suggest ‘transitional waters’ be mentioned in the aim.

 

12. The structure of Section 4.2 confuses me. The story starts with the AMBI. Then several other indices are introduced. Then the AMBI is described in finer details. Then a few recently published indices are cited. Please, make the structure easier to follow or give an introductory sentence, which explains the logical structure of this section.

 

13. line 57, ‘fragile ecotone’. I suggest omitting ‘fragile’ since this descriptor contradicts the following overview showing that the transitional waters are typically inhabited by resilient taxa. ‘Ecotone’ is indeed defined as a transition between two communities, and the term is formally applicable to transitional waters. However, a saltmarsh, fjord, etc. will often have a specific community with specific dominants, which are not a mixture of dominants from the land and sea, and many researches will disagree that these habitats in transitional water bodies are ecotones. Since the term ‘ecotone’ is not essential to the logics of the paper, I suggest omitting the term.

 

14. line 59, “Transitional waters are also often naturally enriched with organic matter making them natural carbon sinks”. The sentence is internally illogical. Change it. Enrichment with organic matter does not make the water body a carbon sink. River water is often enriched with organic matter. But the river bed is typically not the carbon sink. The delta is.

 

15. line 106-119. Please delete two paragraphs of irrelevant text inserted by mistake at the beginning of section 2.

 

16. line 141-145, The text on pristine conditions is correct but lacks, in my opinion, specific examples. Consider adding examples.

 

17. Fig 2. Perhaps add a,b,c markings to the parts of the drawing. What is “species responses to environmental stress present in situ and simulated in the lab (including cellular responses)” is not readily understandable. Think of new wording.

 

18. Table 1 caption is now somewhat misleading because it says the table compiles studies of transitional waters. In fact, the third column does not sufficiently explain what makes the study area belonging to transitional waters. In fact, ‘coral reefs’ (row 2), shelf off Congo (row 3), and others are not examples of transitional waters. Please, restrict the table to transitional waters only and modify the descriptions in the StudySite column to make it clear that a transitional environment is described. Or change the caption so it reads that the table lists all types of habitats where foraminiferal indices have been applied.

 

19. Table 1. Add period after all ‘et al’

 

20. Table 1, row1. “Pressure Source” is probably stress source. “Status” is not clear; living/fossil could be more understandable.

 

21. Table 1, row2. Are “New diseases and coral bleaching” stressors?

 

22. Table 1, row2. Spell Caribbean.

 

23. row 3. Was it oil or drill cuttings (Mojtahid et al. 2006)? Check, please.

 

24. Bouchet et al. 2021: something is wrong with tabulation in this and next rows.

 

Table 1. Make ‘sp. Tolerance’ lower case everywhere.

 

25. Table 1. Correct spelling ‘Meta barcobinf’ (Keeley 2018)

 

26. Section 4.1 starting paragraph (276-285) is loosely written and is difficult to comprehend. Only the second sentence brings solid information. The meaning of the other sentences is vague or flawed. As far as I remember, “low species diversity and high species dominance” nearly always are mutually dependable variables in protistan communities. Therefore, “combining indices” does not add information. The mentioned indices have simple formulas, and I do not understand what makes the calculation complex. I suggest the second sentence is preserved, while the other sentences are rewritten or, better, omitted.

 

27. line 332, ‘algal symbiont organisms’ sounds unusual. Perhaps the authors meant photosymbiont-bearing organisms.

 

28. Section 8 “The way forward.” I personally do not understand what this section is about and what the message is. However, I will not criticize this. Perhaps, some readers will understand this and find it helpful.

Author Response

 

The authors of the manuscript would like to thank each reviewer for their constructive comments, which have certainly helped to improve the quality of the overall document. 

Responses to the reviewer’s comments are in italics and please see the attachment. 

Author Response File: Author Response.pdf