PONE-D-22-17432Otolith geochemistry reflects life histories of Pacific bluefin tunaPLOS ONE

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately 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: Yes

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3. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). 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 ONE 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: This study presents an original research article on otolith trace element profile analysis of Pacific bluefin tuna (Thunnus orientalis), as an approach to provide records of their life history. Authors apply for the first time this technique in Pacific bluefin tuna collected across the species adult distributional range; covering distant areas from the Pacific Ocean (i.e., west, east, and south) and discuss on how different elements provide ontogenetic records of physiological and environmental histories.

Overall, the article is presented intelligibly and is easy to follow. Both experiments and statistics are performed to a high technical standard and are described in sufficient detail, so that other scientist can follow this study. Authors also state that data is available under request without restrictions. Results are rigorously reported and support the conclusions of the article. The motivation behind the work is clearly described, with straight and sound discussion of the observed results and in the limitations of the performed study.

I do believe that this research meets all criteria for publication in PLOS ONE journal. However, there are some minor issues that could be improved in my point of view before its publication as a high-quality manuscript:

- My biggest concern is with the readability of the figures and tables. I don't know if it is a problem with the system, or with the quality of the figures themselves, but they should be thoroughly revised as they are difficult to read as I see them. Please check them for quality standards and size format.

- I think the discussion lacks a little bit more, the microchemistry part is very well detailed and contextualized, but it seems to me a good opportunity to discuss a little bit more about migratory behaviours, contingents and discuss some implications of these findings for the Pacific bluefin tuna management and fisheries as well as and future research priorities. Besides, the introduction of the discussion needs to be refined a bit by looking at the connection between the ideas to be presented later.

If authors can address these minor issues, I do believe that this manuscript will be a great addition to the PLOS ONE articles collection and to the scientific community working with otolith or tuna management related studies. Bellow I have provided specific comments and/or questions to the authors that should be quite straightforward to address. I hope authors and editor can find these suggestions useful, and my congratulations for this nice piece of work, this is good science that needs to be shared!

Introduction

Line 85: I suggest using “core-to-edge” as it is more common in the literature and then in MS you are referring to that part as “edge”.

Lines 83-96: I would add also a small sentence saying that there is also substantial uncertainty on how intrinsic and extrinsic processes affect elemental incorporation into the otolith, and also that responses can be species specific (e.g. Hüssy et al., 2020; Sturrock et al., 2015).

Line 93: You can cite Farwell et al. 2001 at the end of this sentence if you want, which says “The open ocean, pelagic environment of most scombrid species has made it challenging to conduct field research. Their high metabolic rates and specialized swimming result in significant space requirements if held in captivity. The major challenge is that tunas must swim continuously, which makes collecting and captive care difficult”.

Farwell, C. J. (2001). 10. Tunas in captivity. Fish physiology, 19, 391-412.

Line 99: And differentiate among contingents or fish with different life histories?

Line 108-109: I suggest replacing “LA ICP MS” by “LA-ICP-MS”

Line 109: From hatch time to adult?

Line 110: I feel that “comparing complete chemical profiles” would be more accurate than “comparing complete life histories”

Line 114: I suggest deleting “biominerals” at the end of the sentence.

Material and Methods

Lines 118-120: I think it will be nice to indicate here how many otoliths did you get from each region, and not later in Results section.

Line 120: I feel that a map would be a great added value here, where you can show the location of the 3 regions you are considering (instead of figure S1), and the location of the spawning areas. I think this will be a plus for the manuscript and will help the non PBT familiarized readers to locate the regions you mention throughout the manuscript (I needed to check in google maps to get the whole picture in my mind).

Table 1: I think that table 1 needs from some restructuration for the paper, for example, I am not sure if both PBT_ID and Otolith ID are relevant for the reader (perhaps choose only one). Same I am not sure if the fishing methods adds something here? Like this you could use the space you have left over to incorporate a “Region” column where you indicate if samples belonged to WPO, EPO or SPO a with the Location only, readers can be confused (as it was my case because I am not familiarized with the Pacific). Please add to the legend that size is fork length (FL). Also check that are some measures of FL and GG that are in bold.

Lines 129-130: “It was also impossible to know with certainty the migratory histories of sampled fish…” sure, but this is what you want to inspect no? I would suggest deleting this sentence and said only that fish were grouped by sampling region for comparisons.

Figure 1b: Perhaps it is worthy to write core, inflexion point and edge in the figure to help the readers locate the otolith position afterwards? Not sure…

Line 151. Crystalbond “adhesive” or “glue” instead of “cement”?

Line 165: Perhaps “Otolith sections and standards…”

Line 173: Perhaps you can cite Sturgeon et al., 2005 at the end of this sentence.

Sturgeon, R. E., Willie, S. N., Yang, L., Greenberg, R., Spatz, R. O., Chen, Z., ... & Thorrold, S. (2005). Certification of a fish otolith reference material in support of quality assurance for trace element analysis. Journal of Analytical Atomic Spectrometry, 20(10), 1067-1071.

Line 190: Are these mean annual annuli? If so please state it in the text

Line 190: But this image only shows annual rings up to 3 years, how did you do for your older individuals?

Line 197: I know you mention later in the discussion, which is really nice, but I think it would also be worthy to mention here that time frame represented in each individual is different.

Line 200-201: Was your data normally distributed and present homogeneity of variances so that it justifies the use of one way ANOVA? If so please state, if not, consider using another non-parametric test. I see that you mention latter that a Brown- Forsythe test was performed and confirmed that variances of the populations from which the samples are drawn are equal, but what about normal distribution?

Results

Lines 212-216: I am not sure whether this should go here or in M&M, I feel that it does not fit in results, and it fits better in M&M sampling description.

Line 219: “...but it is possible that PBT…” ?

Line 236: Perhaps add “ratios” after “element:Ca”

Figure 2: “solid line represent mean values and shading depicts ± standard deviation across laser distance” I cannot see this in the figure I get. Please check just in case. “dashed vertical lines denote approximate annuli distances for the first 3 years of life…”, I think it will also be beneficial to add where the inflection point will be represented in the transect, as then you mention this in you discussion.

Figure 3: I personally found confusing the fact that horizontal barckets join regions that are not statistically significant, when usually it is the other way around, I would just mark between which there are significant differences.

Table 2: This table need a little bit of restructuring and editing. Please also indicate in the legend that significant P values are highlighted in bold in the table. Also add that inspected regional differences are between WPO, EPO and SPO.

Lines 282-283: I suggest expanding here and also to mention that although classification differences are more or less clear for WPO and EPO there is also some overlap. Also, that SPO is disperse, and not clear grouping can be observed. So, there are 2 SPO with similar values among them, 1 more “EPO like” and 2 more “WPO like”, as you can see in the classification of table 3.

Table 3: I recommend replacing “origin” by “capture” here. Perhaps you can highlight in bold the correct classifications of the table.

Discussion

Lines 296-297: I feel that this sentence is a bit weak as it is, and you should contextualise it more.

Lines 295-307: I think that some cohesion in the first paragraph of the discussion is missing.

Line 303: All of your fish are originated from the WPO no? not only the juveniles

Line 318: I suggest replacing “core-to-rim” by “core-to-edge”

Lines 318-322: Are all of these in the Pacific? Can you specify more on what similarities did you found? (e.g., enrichment/depletion for early life signatures etc.

Lines 322-324: And also continuous transects no?

Lines 325-333: I think you could also discuss here on the importance of the placement of the transect, as some elements do not precipitate equally in the otolith growth axis (you can check Artetxe-Arrate et al. 2021)

Artetxe-Arrate, I., Fraile, I., Clear, N., Darnaude, A. M., Dettman, D. L., Pécheyran, C., ... & Murua, H. (2021). Discrimination of yellowfin tuna Thunnus albacares between nursery areas in the Indian Ocean using otolith chemistry. Marine Ecology Progress Series, 673, 165-181.

Line 365: What individual variability do you see in you fish for early life period of these elements as you are accounting for fish that were born at different years? Do you see some fish with signatures more similar to the East China Sea and other to Sea of Japan reported in Wells et al. 2020? Maybe you can discuss a bit more here

Line 382: Are lower temperatures expected for the WPO than for EPO and SPO? If so please state it

Line 402-404: But are these occasional dives long enough to be recorded in the chemical signature? I don’t think so…

Lines 419-424: We also found that otolith borders were enriched in Zn in comparison with the rest of the otolith for few different tuna species, perhaps because of Crystalbond inclusion, or because the otolith crystal composition of the border. I don’t know if it is worthy to also consider this in small sentence here?

I do miss a little discussion on contingents and migratory behaviour, and also to recap the importance of this knowledge for management (following your intro)

Conclusions

Perhaps recap your objectives and how you answer them with this study

Lines 448-449: Perhaps you can add “although it is often difficult to discern between the two”

Lines 461: And in other fish in general, as these type studies are mostly lacking for any species.

Best luck.

Reviewer #2: Mohan et al. used otolith geochemical transects (core-to-edge) to reconstruct life histories of adult Pacific Bluefin tuna (PBT). They analyzed trace elements in otoliths of adult PBT obtained from the western, eastern, and southern Pacific Ocean to investigate patterns across ontogeny. Results show that some elements (Li:Ca, Mg:Ca, Mn:Ca) were higher during the first 1-2 years and then decreased independently of fish capture location, while other elements (Sr:Ca, Ba:Ca, Zn:Ca) showed a similar pattern in the first 1-2 years but then showed varying patterns likely related to different migration pathways to the capture location. Overall, the manuscript is well written and showcases the utility of otolith geochemical signatures to investigate entire life histories (birth to capture). I have only a few comments that I would like the authors to address before the manuscript can be accepted for publication in Plos One.

The authors only describe the otolith elemental transect data and do not perform any formal statistical testing. It could be worthwhile to consider using a time-series clustering approach analyzing the first 1-2 years and the remaining years to help support the statement that all PBT spawning and nursery areas are located in the EPO and that after ~2 years PBT migrate to different areas.

Using 100 um from the edge as the capture location signature can be very misleading as you discuss in the Discussion section. Why didn´t you consider using individual age-related distance to obtain a edge signature that corresponds roughly to the same time frame in each individual?

Table 1 legend: Change to “Pacific bluefin tuna (PBT) metadata including collection date, region and method;…”

Table1: Why some of the number are in bold?

Line 144: “Otoliths of PBT were sectioned…”

Line 192-193: Please clarify this sentence. As I understand it, you are referring to the distance from the core to age 1, age 2 etc, but can be interpreted as distance between annuli.

Line 357: YOY PBT

Figures 2-4: Need to be substantially improved for publication.

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Reviewer #1: No

Reviewer #2: No

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Otolith geochemistry reflects life histories of Pacific bluefin tuna

PONE-D-22-17432R1

Dear Dr. Mohan,

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.

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Kind regards,

Antonio Medina Guerrero, Ph.D.

Academic Editor

PLOS ONE

Additional Editor Comments (optional):

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 #1: All comments have been addressed

Reviewer #2: All comments have been addressed

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2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

Reviewer #2: Yes

**********

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

Reviewer #1: Yes

Reviewer #2: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). 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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5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE 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

**********

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 #1: The authors have done a great job on the suggested changes, and have argued for the changes they did not see necessary.

For my part I think the manuscript is ready for publication, congratulations on a job well done and thanks for this manuscript on PBF microchemistry!

Reviewer #2: (No Response)

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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.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: No

Reviewer #2: No

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