Space and Time Use of European Eel Restocked in Upland Continental Freshwaters, a Long-Term Telemetry Study

Round 1

Reviewer 1 Report

General comment

Using a RFID-telemetry approach, the authors were able to monitor eels stocked as glass eels in 6 different river over 6 years. Based on these data the authors describe the habitat use and migration activity of the eels in relation to their age or the settled river.

Overall, the MS provides novel insights on the eel habitat use and behaviour during the first years of the continental life phase. From my perspective, the conclusions should be made against the background that the study is limited to a specific habitat type (upland rivers in Belgium). This relates for example on the given suggestion regarding the restocking management.

While reading the manuscript, I wondered if the available data could not be used to estimate eel stock density or stock size. Such estimates would increase the value of the manuscript, as the number of stocked glass eels should be known.

When editing the manuscript for the resubmission, care should be taken to maintain a scientific style of language.

Further comments and suggestion are given in added pdf.

Comments for author File: Comments.pdf

Author Response

Reviewers/Editor comments:

We, the authors of this manuscript, appreciate the reviewer’s valuable comments that helped our manuscript be improved. All of the comments were accepted based on deliberation among the entire authors, and the followings are our responses to each comment. We have also added in Acknowledgments section "The authors sincerely thank the Editor in Chief, the Special Issue Editor and the three anonymous reviewers, whose valuable comments have helped to improve the quality of this manuscript.”

Reviewer #1

General comment

Using a RFID-telemetry approach, the authors were able to monitor eels stocked as glass eels in 6 different river over 6 years. Based on these data the authors describe the habitat use and migration activity of the eels in relation to their age or the settled river.

Overall, the MS provides novel insights on the eel habitat use and behaviour during the first years of the continental life phase. From my perspective, the conclusions should be made against the background that the study is limited to a specific habitat type (upland rivers in Belgium). This relates for example on the given suggestion regarding the restocking management.

We, the authors of this manuscript, would like to thank warmly the referee for its in-depth reviews and very constructive comments. This study is part of a vast local research program which aims to optimize the glass eel restocking practice in order to restore the altered stocks of eels due to the cessation of the feeding of our rivers with young eels and the decline in glass eel recruitment in the North Sea. We are more than 320 km from the North Sea. Eel recruits in this program are monitored by electrofishing (Part I) to assess stocks, survival, growth, developmental stage and health status (pathogens; PCBs, pesticides, toxic metals), and by telemetry (Part II ) using mobile antenna to assess behaviour, mobility and habitat use and fixed antenna placed at river mouths to study escapement phenology. The management made is based on the movements observed through mobile telemetry (change of microhabitats from age 3+) and fixed telemetry (at the age of 5+: the end of December 2022 silver eel individuals begin to leave the rivers). For this, we have added in restocking management suggestion “… according to our experimental conditions, …”.

While reading the manuscript, I wondered if the available data could not be used to estimate eel stock density or stock size. Such estimates would increase the value of the manuscript, as the number of stocked glass eels should be known.

When editing the manuscript for the resubmission, care should be taken to maintain a scientific style of language.

Yes, the density and size of the restored eel stock are dealt with in Part I (sampling by electrofishing) on the ongoing paper which will soon be submitted to Fishes in support of this telemetry study. We also have incorporated all your suggestions to improve the style of the manuscript as suggested by the referee.

In comments and suggestion given in added pdf.

Please check biology and ecology as key words - they might be too general

The authors are grateful to the referee for these very relevant comments. We have changed “biology” to “sedentarisation”, and “ecology” to “resilience” and “extreme floods” for more clarity.

This statement should be supported by a reference.

Authors thank the referee for this comment.

This was added as: [1-7].

This somehow misleading - this statement should include that restocking should be limited to the natural distribution area of eels.

 Authors thank the referee for this very relevant comment.

We improved this by adding in text: “… and located within the natural distribution area of the species [7–12].” Thanks.

This should be checked - if i keep it right in mind there was an article showing the opposite - See Hanel et al (2022) Scientific Reports

Authors agree this very important comment and it has been improved as: "but a novel scenario indicates that a favourable spawning area could also be located east of the Sargasso Sea at the intersection of the Mid-Atlantic Ridge and the seafronts [15]." have been deleted. Chang et al [15] have been replaced by recent and new paper "Hanel et al (2022) numbered as [15]". Many thanks.

“broad” and “unfortunately” as words to delete.

These were removed as suggested by the reviewer. Thanks.

Would delete "at a high level".

It has been done. Thanks.

I suggest to replace cryptic by another term like "undiscovered" and delete "discreet" as a human behaviour related term.

"a cryptic habit and discreet behaviour" have replaced by " an undiscovered habit and behaviour" as suggested by the referee. Thanks.

Do you have a reference for this statement.

We thank the referee for this comment. This has been provided as [24-27].

See below - the latin names for brown trout and  grayling should be given here

Authors thank the referee for this comment, and therefore we have added latin names for these species as: “"brown trout Salmo trutta" and "grayling Thymallus thymallus ".

delete "powerful" and use effective or dominant
We have changed “powerful“ to “dominant “. We thank the referee.

More information on the restocking should be given, total amount of stocked eels, mean lenght/weight; stocking density or origin of the glass eel

These were added as:” "Restocking in the six rivers (total 43 sites) occurred on 21 March 2017 at a density of 2.4 kg ha^-1 from 17.3 kg of glass eels caught on the France's Atlantic coast and imported through a commercial trade company (SAS Gurruchaga Marée, France) (Figure 1). These glass eels had a mean value (± standard error) of 67.0 (± 3.6) mm for the total length and 0.23 (± 0.04) g for the weight. They demonstrated an excellent sanitary status and were free of pathogens [20]." Thanks.

Please check this sentence,

Authors thank the referee for this comment. We have corrected this from “"We identified the tagged eels were identified,"” to "We identified the tagged eels,…"

I suggest to insert subchapters in the result section to increase the comprehensibility.

Authors also thank the referee for this relevant comment. We have added three subchapters in the results as: “3.1. Relative Abundance and Detection Rate”

“3.2. Mobility and Microhabitat Characteristics” and                                                            

“3.3. Influence of Rivers and Floods on Mobility”.   

This sentence is unclear to me - how have productive habitats been identified.

For clarity, we have corrected from "productive habitats identified  during the spring 2022 telemetry session" to "productive habitats identified by their high number of eels detected during the spring 2022 telemetry session". Thanks.

Replace evolution by development.

This has been made (for the figures 2 and 3) as suggested by the reviewer. Thanks.

Would add a second y-axis for the depth, please check if figure B is needed.

Authors also agree this comment and as suggested by the referee, it has been added a second y-axis for the depth, which has improved the figure. Authors choose to keep figure 4B as it well shows the diversity of bottom substrate use in eels 5⁺. Many thanks.

Whether the study really has a high scientific appeal should be judged by the readers. At the beginning of the discussion it should be mentioned what you have done and what is the major outcome.

Authors thank the referee for this relevant comment. For this, we have changed "Our study has great scientific appeal due to its originality, particularly" to "Our study is original, particularly through…" We have also added: "It provided new insights into the eel behaviour and habitat use during their first years of the continental life phase. We have shown the occurrence, the mobility and the microhabitat preference of the restocked eels in a wide diversity of upland riverine ecosystems, and even when habitats were degraded by flooding events.  Given the context of the drastic decline in the upstream natural colonisation process of wild eels, glass eel restocking practice in upland rivers can be deemed an original solution as well as a source of hope for countries further from the sea and located within the species’ natural distribution area [9,10,28]. This practice can enhance the eel local stocks and probably, in the long term, increase silver eel escapement rates through a greater contribution of upland freshwaters to the production of restocked-origin silver eels [7–12]."

delete can be considered a real success - just mentioned that provides detailed insights on the eel behaviour in the investigated rivers

Authors thank the referee for this comment, and we have corrected this from " can be considered a real success" to "provide detailed insights on the eel behaviour in the investigated rivers".

This section should be moved at the end of the discussion dealing with methodological limitations of the study

Authors thank the referee for this comment. However, the authors suggest not to move this paragraph concerning the methodological limits because they consider it useful to present them directly after having presented the high performance of the detection methodology used. Thanks.

replace useful by needed.

This correction was made. Thanks.

From my perspective such a general conclusion can not be made based on the presented data as no control group with an annual stocking was included. Additionally, natural recruits occur every year which causes a specific settlement dynamic in rivers (see for example Feunteun et al. 2003 "A review of the upstream migration and movements in inland waters by anguillid eels. Towards a general theory"

Authors thank the referee for these very relevant comments. Our study areas, as mentioned previously, are not supplied with new natural eel recruits and several rivers are now emptied of their eel stocks. Hence our program which aims to optimize the glass eel restocking practice to restore and conserve the species in our regions already far from the sea, and in the long term contribute to the panmictic stocks which reproduce at sea. We use as a monitoring technique electrofishing for studying eel demographic parameter and health, mobile telemetry for studying behaviour and habitat use, and fixed telemetry with detection antenna placed at the mouth of rivers for studying the phenology of silver eels escaping the rivers. Authors acknowledge the absence of a control group with annual glass eel restocking. This is why we draw this conclusion based on the results gained from observations carried out under our experimental conditions.

We therefore changed in the text: "From the standpoint of restocking management strategy, this means that an aquatic environment..." to "From the standpoint of restocking management strategy, this means according in our experimental conditions that an aquatic environment..." Thanks.

“tothe”

“tothe” has been corrected to “to the”. Thank you.

Corrected Version of fishes-2211636 is attached.

Author Response File: Author Response.pdf

Reviewer 2 Report

This is an interesting paper reporting eel mouvment after restocking and also taking into account a flooding event. The considered area is quiete small (please add scale and orientation on fig 1B) and conclusion should be restricted to the small portions of rivers studied or demonstration should be done to show that same things happens in the entire river bassin. Parag 2.3 : I have a problem with the sentence starting "We scanned 450-2120 m...". You say that you have 2-4 sites per river with a mean of 2 sites (how this is possible ? please explain ?)

Next paragraph : Flood reached a peak of 108.853 m3, what are the peaks the other years (better than comparing with mean annual flow).

Paragraph 2.4 Index given come from auto-citation work ... what is the significance of these indices especially when considering very limited length of river ? One can imagine that values are different if eels go out of the river portion studied. Please give some argument on that.

First line result : "we detected 66% of the 1051 tagged eels". However, rate of detection is between 10 and 30% in Fig2. Not clear.

Please make legend of figure clearer : what is "n" (fig 2A, what are "a" "b" and "ab" in figure 2B and C

However I found it tricky to read the results section and results have to be presented differently to make them clearer. I suggest to put some figure in supp material. Information on the number of eels tagged by river is not clear.

Minor suggestion : ref 15 in introduction is not accepted by the majority of the community and should not be cited as very speculative.

Based on all these point I suggest major revisions to the paper before acceptance.

Author Response

Reviewers/Editor comments:

We, the authors of this manuscript, appreciate the reviewer’s valuable comments that helped our manuscript be improved. All of the comments were accepted based on deliberation among the entire authors, and the followings are our responses to each comment. We have also added in Acknowledgments section "The authors sincerely thank the Editor in Chief, the Special Issue Editor and the three anonymous reviewers, whose valuable comments have helped to improve the quality of this manuscript.”

Reviewer #2: This is an interesting paper reporting eel movement after restocking and also taking into account a flooding event. The considered area is quite small (please add scale and orientation on fig 1B) and conclusion should be restricted to the small portions of rivers studied or demonstration should be done to show that same things happens in the entire river basin.

We, the authors of this manuscript, would like to thank warmly the referee #2 for its in-depth reviews and very constructive comments. Scale and orientation have been added on fig 1B. The conclusion should be limited to the small portions of rivers studied. This is why in the interpretation of certain results we mention "according in our experimental conditions". Indeed, in our methodological approach, we are evolving from upstream (brooks at the head of the Belgian Meuse basin) to downstream on the longitudinal gradient of the Meuse River. We are currently at the stage of the tributaries of the Meuse River. At each stage, we assess the effectiveness of the restocking in terms of the life history of the recruited eels and their health quality (pathogens and pollutants).

Parag 2.3 : I have a problem with the sentence starting "We scanned 450-2120 m...". You say that you have 2-4 sites per river with a mean of 2 sites (how this is possible ? please explain ?)

Authors thank the referee for this relevant comment. This simply means that the sectors scanned in each river (in total 6 rivers) did not have the same length, nor were the number of sectors identical for each river. We have in total 43 sites restocked with glass eels of which in total 14 sites have been scanned. This has been added to the main text.

Parag 2. 3 Next paragraph : Flood reached a peak of 108.853 m3, what are the peaks the other years (better than comparing with mean annual flow).

Authors also thank the referee for this comment. The annual peaks are at least 12 times lower than the peak observed during the 2021 floods which caused numerous human and material losses, without forget the damage in the rivers. The high dispersion of peak flow values annually observed due to the existence of drought years and rainy years motivates us to choose the average annual flow to better summarise flow data and this descriptor was more suitable for comparison with flood flow.

Paragraph 2.4 Index given come from auto-citation work ... what is the significance of these indices especially when considering very limited length of river ? One can imagine that values are different if eels go out of the river portion studied. Please give some argument on that.

Authors thank the referee for this relevant comment. Low values of this index show poor exploitation of the habitat: eels disperse on the longitudinal river gradient in upstream or downstream direction (=ongoing colonization process), and high values show better exploitation of the habitat and its resources as eels cease to extend their home range (=sedentarisation stage). These are well interpreted and integrated into the manuscript. Thanks.

First line result : "we detected 66% of the 1051 tagged eels". However, rate of detection is between 10 and 30% in Fig2. Not clear.

Authors thank the referee for this comment. This simply means that 66% (n=693 individuals) of the 1051 tagged eels were in total detected at least once during the five telemetry sessions (in total data from 5 years). This explains why this overall detection rate is high. It is therefore quite normal for this rate to drop by examining the yearly detection rate or the detection rate by telemetry session. Thanks.

Please make legend of figure clearer : what is "n" (fig 2A, what are "a" "b" and "ab" in figure 2B and C.

Authors thank the referee for these comments. (n) in Fig. 2A indicates for each detection session the cumulative number of eels tagged since 2017. "a" "b" and "ab" in Figures 2B and C, these letters refer to the applied Fisher's exact test. They mean that rivers sharing the same letter are not significantly different (Fisher's exact test: p < 0.05). These are well shown and presented in the Figs and the caption.

However I found it tricky to read the results section and results have to be presented differently to make them clearer. I suggest to put some figure in supp material. Information on the number of eels tagged by river is not clear.

Authors thank the referee for this comment. We have a huge telemetry tracking database that needed to be summarized and it wasn't as easy for us to do it in this manuscript format. Information on the number of eels tagged per river is summarized and presented in Fig. 2C.

Minor suggestion : ref 15 in introduction is not accepted by the majority of the community and should not be cited as very speculative.

Authors thank the referee for this comment. We have deleted it in text and reference list.

Based on all these point I suggest major revisions to the paper before acceptance.

Thanks for your valuable input.

Revised version of fishes-2211636 is attached.

Author Response File: Author Response.pdf

Reviewer 3 Report

Dear Authors,

I reviewed the manuscript entitled "Space and Time Use of European Eel Restocked in Upland Continental Freshwaters, a Long-term Telemetry Study" finding the work interesting, well prepared and well exposed. The sampling design is well orchestrated and the exposition of the results is also well, despite sometimes it is difficult to follow the flow of the description. 

The results are also well discussed. There are few indications reported below, but it is my opinion that the manuscript can be accepted after a Minor Revision. 

Page 5, chapter 2.2,

line 9: can you provide a refererence for the used anesthetic? Usually in fish sampling MS-222 is widely used. Please if you have a reference for eugelol, add it. 

Line 11: Please rephrase deleting ripetitions

Page 6, chapter 2.5,

line 6: Please replace "test" with "coefficient"

lines 9-11: The FET provides a p-value, corrected for multiple testing hypothesis, associated with whether an annotation category. Can you explain more in detail how you organized the comparisons? 

Chapter 3, last line of the page: here and in the whole manuscript, you can simply report p<0.001

Author Response

Reviewers/Editor comments:

We, the authors of this manuscript, appreciate the reviewer’s valuable comments that helped our manuscript be improved. All of the comments were accepted based on deliberation among the entire authors, and the followings are our responses to each comment. We have also added in Acknowledgments section "The authors sincerely thank the Editor in Chief, the Special Issue Editor and the three anonymous reviewers, whose valuable comments have helped to improve the quality of this manuscript.”

Reviewer #3: I reviewed the manuscript entitled "Space and Time Use of European Eel Restocked in Upland Continental Freshwaters, a Long-term Telemetry Study" finding the work interesting, well prepared and well exposed. The sampling design is well orchestrated and the exposition of the results is also well, despite sometimes it is difficult to follow the flow of the description.

The results are also well discussed. There are few indications reported below, but it is my opinion that the manuscript can be accepted after a Minor Revision.

We, the authors of this manuscript, would like to thank warmly the referee #3 for its in-depth reviews and very constructive comments. Again, thank you very much.

Page 5, chapter 2.2,

line 9: can you provide a refererence for the used anesthetic? Usually in fish sampling MS-222 is widely used. Please if you have a reference for eugelol, add it.

Authors thank the referee for this comment. References for eugenol were added as: “[9-12]”.

Line 11: Please rephrase deleting repetitions

Authors agree this comment and correction has been made. Many thanks.

Page 6, chapter 2.5,

line 6: Please replace "test" with "coefficient"

The authors thank the referee for this comment. This change has been made.

lines 9-11: The FET provides a p-value, corrected for multiple testing hypothesis, associated with whether an annotation category. Can you explain more in detail how you organized the comparisons?

Authors thank the referee for this comment. Here we present how we have organised in R the paired comparisons between the six rivers (A, B, C, D, E and F) e.g. relative abundance for detected eels 5+ (n = 174). (see in Fig. 2B).

For example of comparison between A (=1 in column) and E (=2 in column) rivers

> .Table <- matrix(c(97,77,28,146), 2, 2, by row=TRUE)

> dimnames(.Table) <- list("rows"=c("1", "2"), "columns"=c("1", "2"))

> .Table  # Counts

    columns

rows  1   2

   1 97  77

   2 28 146

> fisher.test(.Table)

Fisher's Exact Test for Count Data

data:  .Table

p-value = 9.007e-15

alternative hypothesis: true odds ratio is not equal to 1

95 percent confidence interval:

  3.871076 11.278261

sample estimates:

odds ratio

6.529.561

Chapter 3, last line of the page: here and in the whole manuscript, you can simply report p<0.001

Authors thank the referee for this comment. However, authors suggest presenting the precise value of p for KW test.

See in attachment revised version of fishes-2211636

Author Response File: Author Response.pdf

Round 2

Reviewer 1 Report

Many thanks for the conducted revision - from my perspective the manuscript can be published in the current form.

Reviewer 2 Report

Please make legend of figure clearer : what is "n" (fig 2A, what are "a" "b" and "ab" in figure 2B and C.

 Authors thank the referee for these comments. (n) in Fig. 2A indicates for each detection session the cumulative number of eels tagged since 2017. "a" "b" and "ab" in Figures 2B and C, these letters refer to the applied Fisher's exact test. They mean that rivers sharing the same letter are not significantly different (Fisher's exact test: p < 0.05). These are well shown and presented in the Figs and the caption.

This part is still not clearly explained in the caption of the figure. Please make it clearer before publication

Author Response

Dear Reviewer 2,

Many thanks for this relevant comment. 

We have corrected for clarity in the legend of Figure 2 as follows:

"(n) indicates the cumulative number of eels tagged during all fall electrofishing sessions performed prior to each spring detection session.", and

"Rivers sharing at least one common letter are not significantly different (Fisher's exact test: p < 0.05)."

Author Response File: Author Response.pdf