Positive Welfare for Fishes: Rationale and Areas for Future Study

Round  1

Reviewer 1 Report

On the whole this is a very interesting paper and i congratulate the authors on a great MS. They provide a nice overview of positive welfare in animals in general and then attempt to apply this criteria (or illustrate how it could be applied) to fishes. They identify multiple potential future research avenues. 

The work is very well written.

Perhaps the weakest part of the paper is the section on play which is reasonably controversial outside of mammals simply because we struggle to recognise it. I think it is hardest of all in fish.  Much of the criteria outlined in this section is subjective and thus it makes it very difficult to see how we can move forward. At best, the evidence for play in fish is anecdotal and i suggest the authors should state this upfront. I did pick out one or two eras where we really could formulate a testable hypothesis and perhaps there needs to be more emphasis placed on these instances.

Ive made several suggestions and comments on the MS. 

Comments for author File: Comments.pdf

Author Response

Reviewer 1:

Below please find the reviewer comments as well as indications to how we have revised the manuscript in response. The reviewer comments are in grey Garamond font, our responses are in black Garamond font. We have also added in-line comments from the reviewers to the Word document and noted all changes to the manuscript with the “track-changes” function in Word.

R1.1: On the whole this is a very interesting paper and i congratulate the authors on a great MS. They provide a nice overview of positive welfare in animals in general and then attempt to apply this criteria (or illustrate how it could be applied) to fishes. They identify multiple potential future research avenues. 

The work is very well written.

Thank you for these encouraging words about our work and for the suggestions regarding ways we can improve our MS.  The in-line comments, our responses and subsequent content edits are recorded in the revised manuscript and some are also available below. Please see the revised manuscript with tracked changes for grammatical and formatting corrections as well. 

R1.2: Perhaps the weakest part of the paper is the section on play which is reasonably controversial outside of mammals simply because we struggle to recognize it. I think it is hardest of all in fish.  Much of the criteria outlined in this section is subjective and thus it makes it very difficult to see how we can move forward. At best, the evidence for play in fish is anecdotal and i suggest the authors should state this upfront. I did pick out one or two eras where we really could formulate a testable hypothesis and perhaps there needs to be more emphasis placed on these instances.

            We agree with the reviewer regarding the difficulty of identifying play in general and the great difficulty of identifying play in fish specifically.  Accordingly, we have substantially edited the entire play section and now include more discussion of the inherent limitations of studying whether a behavior in another species really is play and highlight the anecdotal nature of much of the existing evidence of play in fishes.  We have also deleted much of our discussion of anecdotal accounts of play.  Please see our updates beginning on line 424 in the revised MS.

R1.3: (in-line comments)

We found the in-line comments to be highly valuable and have noted the reviewer suggestions as comment bubbles in Word and modified the MS accordingly. 

Author Response File: Author Response.docx

Reviewer 2 Report

Dear Authors,

The present paper can be considered a Review-State of the Art in Positive Welfare applied to fish.

In overall, I find the paper interesting to read and well written but too long and not completely focus on fish.

Since I do not have the text with numbered lines I will perform some general recommendations.

·       “The aims of the review” appear in Conclusions section and they must go after the Introduction.

·       I recommend authors to synthetize the paragraphs containing information regarding human-animal ethology and focus in explaining more deeply the ones related to fish.

·       I recommend authors to build 2 tables: one for fish related info and the other for animal-human info. Those tables will link the different author’s studies with the different topics.

·       I feel that a reference is needed when speaking about the 5 Freedoms. I recommend the Brambell Report 1965.

·       Since Fish Welfare strongly is linked with aquaculture due to the fact that it affects final product’s quality I feel obligatory to address it in the text and to show more examples related with that topic.

·       Some sentences need to be rewritten:

o   “Existing evidence...” --> no reference afterwards.

o   “there are several studies...” --> and only 1 reference afterwards.

o   “multiple studies...” --> and only 1 reference afterwards.

o   “We suggest investigating...” --> must go in the Conclusions.

o   “Cod (Gadus morhua)” --> Gadus morhua must be in italics.

o   “Anecdotal reports indicate...” --> reference needed.

Author Response

Reviewer 2

Below please find the reviewer comments as well as indications to how we have revised the manuscript in response. The reviewer comments are in grey Garamond font, our responses are in black Garamond font. We have also added in-line comments from the reviewers to the Word document and noted all changes to the manuscript with the “track-changes” function in Word.

R2.1: The present paper can be considered a Review-State of the Art in Positive Welfare applied to fish. In overall, I find the paper interesting to read and well written but too long and not completely focus on fish.

Since I do not have the text with numbered lines I will perform some general recommendations.

Thank you for your interest in our work and drawing our attention to the need to tighten up parts of our MS (see, in particular, the section on play which has been substantially reduced and clarified, beginning line 446).  We apologize for not including numbered lines and have corrected this oversight for the revision of the MS.

R2.2: “The aims of the review” appear in Conclusions section and they must go after the Introduction.

We have removed the aims of the review from the conclusion and added them to the introduction.

R2.3: I recommend authors to synthetize the paragraphs containing information regarding human-animal ethology and focus in explaining more deeply the ones related to fish.

           Thank you for this recommendation to make the MS more appealing to fish researchers.  We have worked on condensing the non-fish ethology work throughout the MS and expanding the fish work.  Part of our reliance on non-fish research was out of necessity, however, as there has been comparatively less done on positive fish welfare.  In addition, we believe that noting the parallels across the animal kingdom (including humans) strengthens the basic science contribution of the work by contextualizing the patterns found in fish within a broader field of research.  Nonetheless, we are sensitive to the need to keep the focus clearly on fish and have thus tried to increase the ratio of fish:non-fish research throughout. 

R2.4: I recommend authors to build 2 tables: one for fish related info and the other for animal-human info. Those tables will link the different author’s studies with the different topics.

        We found this to be a valuable suggestion and attempted to construct such a table, but it ended up being somewhat redundant with information contained in the text (which already has a fairly formulaic structure).  Moreover, as such tables are more typical of systematic reviews, we are concerned that it might give some readers the impression that the references contained within are exhaustive (when in fact they would only be a subset of studies that we found to be useful exemplars of our central points).  At the Editor’s discretion, therefore, we would prefer to leave this idea for future publications, though we wholeheartedly agree that a thorough and complete version of such a table would be a valuable contribution to the literature.

R2.5: I feel that a reference is needed when speaking about the 5 Freedoms. I recommend the Brambell Report 1965. 

The recommended reference has been added.

R2.6: Since Fish Welfare strongly is linked with aquaculture due to the fact that it affects final product’s quality I feel obligatory to address it in the text and to show more examples related with that topic.

            While we agree that welfare and product quality may often be linked, we also believe that it is important to note that they are distinct variables.  For example, it is possible that certain improvements to welfare would not improve overall product quality or production efficiency.  Even without these quality improvements, however, it would still be necessary to consider the welfare improvements for their own sake.  The distinction between production and welfare may be especially true for positive welfare considerations.  Thus, at the Editor’s discretion, we would prefer leaving the connections between welfare and production to future researchers as our present focus on welfare as an end-goal with stand-alone value is a central aspect of our paper. 

R2.7: Some sentences need to be rewritten:

·      “Existing evidence...” --> no reference afterwards.

·      “there are several studies...” --> and only 1 reference afterwards.

·      “multiple studies...” --> and only 1 reference afterwards.

·       “We suggest investigating...” --> must go in the Conclusions.

·      “Cod (Gadus morhua)” --> Gadus morhua must be in italics.

·      “Anecdotal reports indicate...” --> reference needed. 

We have implemented these edits (some of which were also noted by other reviewers) in the revised manuscript. Thank you very much for your careful attention to and help with improving our contribution.

Author Response File: Author Response.docx

Reviewer 3 Report

This was quite interesting review paper as the authors have taken a non-conventional view to animal welfare. I was not familiar with the concept of positive welfare, and I was really wondering first that what this all is about. Thus, the term positive welfare would need some explanation in the abstract. In the main text you have described this term only in the second chapter but you talk about it already at the very beginning. Thus, this would need some re-organizing or clarification so that the reader would not lose interest right at the beginning.

In the abstract you state “we also suggest ways forward in developing accurate and appropriate positive welfare indicators for fish.” and in conclusions “we suggest ways in which caretakers can promote positive welfare in captive fish”. However, both these suggestions remain unclear for me. Could you please summarize your suggestions in a table or in text with concrete examples using e.g. bullet points?

For me it remains somehow unclear whether this article is aimed only for only researchers or also for potential end users of fishes, such as fish farmers/aquaculturists (or as you say “caretakers”). From fish farmer point of view this article would be of very little interest, as it has no concrete suggestions how the environment should or could be improved. Most experiments you cite have likely been done only with a few fishes only – what will happen if there are e.g. 50 – 100 kg of fish per m3 of water. I was kind of surprised that environmental enrichment in aquaculture settings has not been mentioned in text at all.

I attach a pdf with lots of minor comments. In general, the text reads very well. However, you must pay attention to write it in correct scientific manner: use scientific names for species and add publication year to all citations. Make sure that the alignment of text is similar throughout the ms. I would like you to refrain from referring to humans as animals. You must do quite some work with the reference list: now it is a pot-pourri of different kinds of formats.

Comments for author File: Comments.pdf

Author Response

Reviewer 3

Below please find the reviewer comments as well as indications to how we have revised the manuscript in response. The reviewer comments are in grey Garamond font, our responses are in black Garamond font. We have also added in-line comments from the reviewers to the Word document and noted all changes to the manuscript with the “track-changes” function in Word.

R3.1: This was quite interesting review paper as the authors have taken a non-conventional view to animal welfare. I was not familiar with the concept of positive welfare, and I was really wondering first that what this all is about. Thus, the term positive welfare would need some explanation in the abstract. In the main text you have described this term only in the second chapter but you talk about it already at the very beginning. Thus, this would need some re-organizing or clarification so that the reader would not lose interest right at the beginning.

Thank you for drawing our attention to this very important point! We have now included a definition of positive welfare in the Abstract and the first sentence of the Introduction.  The definition of positive welfare that we used was: “mental and physical states that exceed what is necessary for immediate survival”. 

R3.2: In the abstract you state “we also suggest ways forward in developing accurate and appropriate positive welfare indicators for fish.” and in conclusions “we suggest ways in which caretakers can promote positive welfare in captive fish”. However, both these suggestions remain unclear for me. Could you please summarize your suggestions in a table or in text with concrete examples using e.g. bullet points?

            This comment has made us realize that our intended contributions were not described with precision in the Abstract or the Conclusion.  We have modified these passages (see line 23 and line 531) to clarify our goal in compiling this research, which was, more specifically, to identify areas for future research that would support the development of standard codes of practice for and indicators of positive welfare in fish.  At this time, there is not a large enough body of scientific knowledge to generate well-supported assessment paradigms and targets of positive fish welfare.  Instead, we hope this review will stimulate the collection of such data while also mapping out promising ways forward.  Nonetheless, the existing literature does contain some intriguing indications of potential ways to provide and identify positive welfare in fishes.  In our revised MS, therefore, we have made sure to highlight such opportunities where possible (see, for example, line 522 and line 534). 

R3.3: For me it remains somehow unclear whether this article is aimed only for only researchers or also for potential end users of fishes, such as fish farmers/aquaculturists (or as you say “caretakers”). From fish farmer point of view this article would be of very little interest, as it has no concrete suggestions how the environment should or could be improved. Most experiments you cite have likely been done only with a few fishes only – what will happen if there are e.g. 50 – 100 kg of fish per m3 of water. I was kind of surprised that environmental enrichment in aquaculture settings has not been mentioned in text at all.

            Thank you also for calling our attention to the ambiguity in our intended audience and the need to include reference to the literature on environmental enrichment practices in aquaculture settings.  We now have added a discussion of this literature (beginning line 271):

Providing fish with environmental enrichment [48] designed to increase complexity while mimicking their natural habitat may be an effective way to offer choice, encourage exploration, and facilitate curiosity.  While determining appropriate enrichment strategies is highly dependent on the species’ natural history, there are some principles that have been found to be successful in generating positive effects on a variety of species used in research and aquaculture.  In general, many species of captive fish benefit from the incorporation of species-appropriate substrate, tank color, structural complexity and sensory stimulation provided by aquatic plants, submerged structures such as logs or rocks.  For a comprehensive overview of current environmental enrichment research for captive fishes, see Naslund and Johnsson, 2016 [48].

Similarly, we have also made modifications throughout the MS to highlight opportunities for aquaculture (see, for example, line 273) because we believe that the principles we discuss are relevant to all captive fish and their managers.  While the implementation challenges for positive welfare may be unfamiliar and/or less well-researched in traditional aquaculture settings, many of the ideas would not be impossible or even particularly costly to implement (e.g., self-feeding apparatus).  Importantly, beyond specific recommendations, we believe that the concept of and rationale for positive welfare should be on the radar of fish farmers as it is likely to become an increasingly important issue for the industry and having forewarning of such developments may be useful for future facility design and planning for example. 

R3.4: I attach a pdf with lots of minor comments. In general, the text reads very well. However, you must pay attention to write it in correct scientific manner: use scientific names for species and add publication year to all citations. Make sure that the alignment of text is similar throughout the ms. I would like you to refrain from referring to humans as animals. You must do quite some work with the reference list: now it is a pot-pourri of different kinds of formats. 

Thank you very much for the detailed notes and corrections regarding the editing and reporting errors/inconsistencies in our MS.  We have implemented the in-line corrections and suggestions.  We would, however, prefer to retain occasional indications to reflect the biological fact that humans are a species of animal, though we have tried to minimize these references whenever possible.  Our modifications to the in-line comments can be viewed using “track-changes”.

Author Response File: Author Response.docx

Reviewer 4 Report

In this paper, the authors merged what is already known about positive welfare with existing fish behavior research in order to develop a plan of action for fish, also contributing to the development of positive welfare standards and assessment strategies for fish. Furthermore, authors suggested ways forward in developing accurate and appropriate positive welfare indicators for fish. 

The review represent an important starting point for future research in fish welfare. For this reason, this manuscript deserve to be published after minor revision.

Numbered lines on the side of the paper are missing. It doesn't help the reviewer's suggestions.

I think that authors should be better observe the authors guidelines of Fishes, since all references all not well written. For example, you should cite a journal articles as follow: Author 1, A.B.; Author 2, C.D. Title of the article. Abbreviated Journal Name Year, Volume, page range. Available online: URL (accessed on Day Month Year). 

In paragraph 5.1 "Identifying and Assessing Play in Fishes" you cite "Burghardt, 2005", but you didn't use the reference number in square brackets [ ] every time you cited it. 

The same is true for the following sentence: "coloration changes (Siebeck, 2004), electrical impulse (Friedrick, 2006; Bullock & Hopkins et al., 2005), and bioluminescence" (page 7, paragraph 4.2). Siebeck, 2004, Friedrick, 2006; Bullock & Hopkins et al., 2005 are also omitted in the reference list. Authors must check all citations and references before to resubmit the manuscript

Author Response

Reviewer 4

Below please find the reviewer comments as well as indications to how we have revised the manuscript in response. The reviewer comments are in grey Garamond font, our responses are in black Garamond font. We have also added in-line comments from the reviewers to the Word document and noted all changes to the manuscript with the “track-changes” function in Word.

R4.1: In this paper, the authors merged what is already known about positive welfare with existing fish behavior research in order to develop a plan of action for fish, also contributing to the development of positive welfare standards and assessment strategies for fish. Furthermore, authors suggested ways forward in developing accurate and appropriate positive welfare indicators for fish. 

The review represent an important starting point for future research in fish welfare. For this reason, this manuscript deserve to be published after minor revision.

Numbered lines on the side of the paper are missing. It doesn't help the reviewer's suggestions.

Thank you for your encouragement about our approach and for drawing our attention to the line-numbering oversight.  We apologize for the unnecessary difficulties it caused during the review process.  Line numbers are included in revised manuscript.

R4.2: I think that authors should be better observe the authors guidelines of Fishes, since all references all not well written. For example, you should cite a journal articles as follow: Author 1, A.B.; Author 2, C.D. Title of the article. Abbreviated Journal Name Year, Volume, page range. Available online: URL (accessed on Day Month Year). 

We apologize for these formatting issues and have gone through our reference list to double-check that they adhere to the author’s guidelines of Fishes.

In paragraph 5.1 "Identifying and Assessing Play in Fishes" you cite "Burghardt, 2005", but you didn't use the reference number in square brackets [ ] every time you cited it. 

The same is true for the following sentence: "coloration changes (Siebeck, 2004), electrical impulse (Friedrick, 2006; Bullock & Hopkins et al., 2005), and bioluminescence" (page 7, paragraph 4.2). Siebeck, 2004, Friedrick, 2006; Bullock & Hopkins et al., 2005 are also omitted in the reference list. Authors must check all citations and references before to resubmit the manuscript

We have gone through the MS and corrected these mistakes—thank you for taking the time to alert us to this issue. 

Author Response File: Author Response.docx

Round  2

Reviewer 2 Report

Although some suggestions are not included, the manuscript is overally performed. I recommend to accept it in the present form.

Author Response

Thank you for your thorough and excellent review of our manuscript. Your suggestions and revisions were much appreciated! 

Reviewer 3 Report

I was very happy with this new improved version. It is very nice now. I found a couple of typos which you should corrected for the final version:

L. 234: niloticus

L. 236: O. mossambicus

L. 326: phoxinus

L. 327: Delete Danio rerio (has been mentioned earlier)

L. 348: Näslund

L. 482-484: there must have been a misunderstanding in my earlier comment. I meant here that you should tell shortly about the "example of a positive contrast": what kind of a finding was this? What did the fish do?

L. 565-567. I suggest the following change: "For example, Burghardt (2005) [14] describes an instance in which a communally‐housed white spotted cichlid (Tropheus duboisi; a cichlid from Lake Tanganyika) was observed repeatedly approaching a cichlid species from Lake Malawi (Labeotropheus sp.), ..." Delete a parenthesis from the end of the sentence.

L. 578. In my earlier review I asked for details for "tuna and sharks". These both are large groups of different kinds of fishes, so please do not generalize too much but give species names which are known to do the object play.

I want to congratulate the authors for the nice review. 

Author Response

Thank you for your swift and thorough review of our manuscript. We very much appreciate your feedback! Please see our full response letter attached. 

Author Response File: Author Response.docx