Evidence for Aviculture: Identifying Research Needs to Advance the Role of Ex Situ Bird Populations in Conservation Initiatives and Collection Planning

Round 1

Reviewer 1 Report

This is a very interesting article, I read it with interest and did not find anything to comment on.

I recommend accepting for publication.

Author Response

Thank you for the positive comments. I am pleased that you enjoyed the paper and found it useful. 

Reviewer 2 Report

I found the paper very interesting, developing for birds the previous more general work about animals kept in zoos (Palgrave Communications, 2019. 5: 1-10). The text is well written and organized, and Table 1 specially well-done and usefult. I perhaps miss an additional figure summarizing the results presented in lines 357-391. There are many sections and percentages here, and the reader might get lost among them.

Author Response

Thank you for the comment. I have drawn a new figure to explain the results within this section.

Reviewer 3 Report

This is a very good paper and approaches the topic of ex-situ conservation and related issues in a good and integrated fashion, making useful proposals on how such integration may work.

Apart from a few minor spelling erros or word omissions (e.g. Line 23 wild-welling—wild-dwelling; Line 26  can gained= can be gained; Line 431--- o you mean ‘changes’ or ‘chances’?),  there is little I feel requires any queries or correction.

However, the conclusion, especially the first two sentences (lines 425-428) are outrageously inappropriate and turn biology and everything we known on its head. It states that zoos have a pivotal role in advising conservation programs! I would have thought that the opposite is the case and that zoos should take the lead from the field.  I would have thought that zoos should become more conversant with research studies of behaviour of birds as observed in the field, surely, so that housing, enrichment and multispecies asemblages become a little more species appropriate!  As a personal comment: I have yet not seen a single well adjusted and ‘happy’ bird in a zoo but plenty of those in the wild. Countless studies suggest very strongly that zoo reared animals have a far lower chance of survival post release than wild-reared same age conspecifics – we know also that captivity creates its own paradigms and encourages behaviours which may or may not be known in the wild or even be useful in the wild. Where on earth do the authors derive the notion that zoos can be useful in informing field-workers??

And what are trained aviculturalists? In my experience of local knowledge (admittedly may be different in other countries) , they run the business of breeding birds for the pet market and the standards of care of the facilities I have seen were minimalist at best and successes solely geared to producing a sellable product. Are these ‘trained aviculturalists’ equipped with a degree in ethology and/or biology? Or have they done college courses in husbandry? In my experience, at best it has been the latter (I know of aviculturalists without any training of any kind who simply started this as a hobby and became rather good at their task) and if this is so, I feel that university trained field ornithologists might very much take umbrage at the statements made in these lines and read it either as utter arrogance or as complete ignorance of the findings of how captive populations compare (poorly) to wild-born extant species…

Our general understanding is that zoos have yet a lot to learn (and be sufficiently interested in research and in such knowledge, as many are not) about their avian displays, their needs, behavioural repertoire, cognitive dimensions, emotions and the needs for interactions of the kind that are meaningful within that species. In many debates it has become clear that zoo staff are generally not familiar with the latest known factors affecting behaviour and the subtleties of their physiological, hormonal, cognitive and affective dimensions of birds. Of course, that too varies from country to country and, as in all fields, there may be a few outstanding and unbiased research efforts going on but this is so far not the case in a substantial number of zoos.

If this reviewer has misunderstood the intention, apologies, but if this reviewer reads it this way so would others most likely too.. The conclusion is truly awful because it is political, playing to certain parties rather than staying within the science.

Until the conclusion is fixed, I could not possibly recommend this paper for publication because of the way the conclusion is framed. It makes a mockery of biology, of the knowledge we have of the stark differences between captive and wild populations of birds which, ultimately, suggests that the conclusion is not based on science.  

Author Response

Thank you for the comments. 

I have rectified each of the spelling and typographical errors.

I have re-written the conclusion to explain that I am referring to accredited institutions (e.g. AZA, EAZA, BIAZA collections). I have further included examples in the conclusion that explain the role of the ex situ population to global conservation action, and that it is the knowledge possessed by trained professional staff that can help with One Plan Approaches to conservation. I have stipulated that accredited institutions are in the introduction.

I have explained some of the challenges noted with ex situ conservation and I have further expanded on some of the research areas in table 1 to show the need for welfare considerations that can impact on conservation output (i.e. a zero tolerance approach to abnormal repetitive behaviour). This has been included in the conclusion too. I have added in further information that shows the benefits of trained zoo professionals to best practice management. 

I have explained that collaboration between ex situ facilities and in situ conservation organisations has resulted in reintroduction and down listing of Red List status for particular species of bird, and I have made the call for continued research into the ecological needs of species housed in captivity so such approaches can become more commonplace.  

I have edited to ensure that I refer to zoo aviculturists, not those breeding for the pet trade. 

I have edited the abstract to show that research from the wild is useful for furthering captive care. 

Just as an aside, I teach zoo professionals across a range of courses, from the accredited diploma from the UK's zoo governing body, to BSc and MSc level courses. The modern day zoo keeper is highly trained and is expected to have a higher level qualification upon entry into the role. Keepers are instilled with a whole range of knowledge and expertise that are integral to husbandry and conservation. Through my work at WWT, I have seen how the conservation and recovery of the Madagascar pochard would not have been successful without the skills of the bird keepers who knew how to raise ducklings, how to match pairs together for successful courtship and how to build release cages out in the field that allowed the birds to feed and forage as normal. Throughout this article I have stressed the need for collaboration between field based and ex situ partners. I am sorry to read that this call for a communal effort comes over as arrogant. 

Round 2

Reviewer 3 Report

Review second round (comments to author) 

The paper overall is very informative and one that will create great interest because it has provided very detailed and useful information and the corrections made and information provided in the response to the review have helped persuade this reviewer that this is a very good paper written not to offend and make exaggerated claims but to provide detailed information.

There still is a problem with the Conclusion (Lines 434-438).  These lines are still propagandist rather than science, opinion rather than based in facts and must go because the generalisations are massively overdrawn. There are about 10,000 zoos worldwide, many of them in private hands. To my knowledge, organisations such as the World Association of Zoos and Aquariums (WAZA) and Species360 (with about 1,100 members) capture only a fraction of zoos. . - I grant the author that a few zoos (0.1% -0.5% of zoos worldwide perhaps) have actually achieved what is claimed here and when one belongs to an environment in which that 0.1% applies, one may well be proud of and convinced of the reality of what is being argued here. Even the Smithsonian, a very well-funded institution, will just begin the process of learning and accommodating native avian species towards the last quarter of 2021. All this is relatively new and the charge is made, possibly in the right direction, by a handful of zoos but it is not representative nor is there sufficient proof of successful reintroductions of a sufficiently large number of species to proclaim zoo leadership in conservation!

Leaving out those first few sentences in no way diminishes what has been argued in the paper. It shines through loud and clear that the author is proud of the actions in his environment (and may well be rightly so) and convinced of the zoo’s importance and of a future role for zoos generally in conservation and the author appears to have a clear idea on how this can be achieved. Moreover, the author’s reply to the first round of the review process also showed that the author’s particular environment may well be ahead of the pack-- and possibly a good way ahead-- in terms of training and definitive plans for implementation. Solid research training (at doctoral level) is in place and this alone is very promising.  Obviously, a thorough education is an essential prerequisite for establishing a culture of research and generating a reliable and pertinent, non-trivial (and believable) in-depth data collection. I know of zoos (currently) that are research hostile, research incapable and, at the lowest level, do not even have basic record keeping of its animals, a task that requires no more than a change in attitude and policy. No doubt, advanced zoo environments may and must take the lead among zoos, not necessarily in conservation. However, it is dangerous at this point to make a case AS IFzoos generally were at this stage and of any use to conservationists or reintroductions. The cynics have argued that zoos needed to find a new raison d’être, a way of showing their relevance in the modern world and piggybacking onto a publicly accepted goal of conservation that, as cynics argue, in most cases is unlikely to be reached but a good marketing strategy for the time being. I am sure that the author does not want to give the cynics more fuel for their arguments.

Further- to be ethically responsible in the promotion of ideas as this paper offers, is to understand how few projects in the model proposed in the paper have actually succeeded in practice. I take the (more modest) view of the Smithsonian which seems a genuine and achievable goal, that zoos need to learn what birds actually need in order to live and survive in the wild and that the passenger pigeons could not be saved because no-one knew how to look after them.

If these changes to the ms are made in full, I have no hesitation in recommending this paper for publication.

SOME ADDITIONAL CORRECTIONS:

Line 353/54 --- “with a final search in January 2019 for any December 2018 that may have been published”.  ”for any December 2018”??  something missing here-sentence does not make sense

Line 420 —‘to provide an evidence’- drop “an”

And in the References  

Quite a few references are incomplete short hand (as if written only to an initiated few) and need to be completed; e.g.. Refs 5,11-14 , 33, 52 -54, 79,80,82 –the most minimalist and entirely obscure entry is “EAZA. About us. 2021.”

Any such entries must be completed:

First) All abbreviations must be spelled out in full first – no CPSG, BIAZA, CBD –  may be enough for a specific in-group but the readership for the journal to which this paper has been submitted is for a wider audience - –

Second): publications of books and pamphlets and other promotional material must have a place and publisher even  when produced internally (i.e. even if authorship and publisher are the same  or, if only produced online, provide the full website details)

Third) Ref. 15 (Redondo) is obviously a thesis and it must state so (Doctoral thesis, University Exeter)—include also place and country—there are several ‘Exeter’ places in the world.  

Author Response

There still is a problem with the Conclusion (Lines 434-438).  These lines are still propagandist rather than science, opinion rather than based in facts and must go because the generalisations are massively overdrawn. There are about 10,000 zoos worldwide, many of them in private hands. To my knowledge, organisations such as the World Association of Zoos and Aquariums (WAZA) and Species360 (with about 1,100 members) capture only a fraction of zoos. . - I grant the author that a few zoos (0.1% -0.5% of zoos worldwide perhaps) have actually achieved what is claimed here and when one belongs to an environment in which that 0.1% applies, one may well be proud of and convinced of the reality of what is being argued here. Even the Smithsonian, a very well-funded institution, will just begin the process of learning and accommodating native avian species towards the last quarter of 2021. All this is relatively new and the charge is made, possibly in the right direction, by a handful of zoos but it is not representative nor is there sufficient proof of successful reintroductions of a sufficiently large number of species to proclaim zoo leadership in conservation!

Leaving out those first few sentences in no way diminishes what has been argued in the paper. It shines through loud and clear that the author is proud of the actions in his environment (and may well be rightly so) and convinced of the zoo’s importance and of a future role for zoos generally in conservation and the author appears to have a clear idea on how this can be achieved. Moreover, the author’s reply to the first round of the review process also showed that the author’s particular environment may well be ahead of the pack-- and possibly a good way ahead-- in terms of training and definitive plans for implementation. Solid research training (at doctoral level) is in place and this alone is very promising.  Obviously, a thorough education is an essential prerequisite for establishing a culture of research and generating a reliable and pertinent, non-trivial (and believable) in-depth data collection. I know of zoos (currently) that are research hostile, research incapable and, at the lowest level, do not even have basic record keeping of its animals, a task that requires no more than a change in attitude and policy. No doubt, advanced zoo environments may and must take the lead among zoos, not necessarily in conservation. However, it is dangerous at this point to make a case AS IFzoos generally were at this stage and of any use to conservationists or reintroductions. The cynics have argued that zoos needed to find a new raison d’être, a way of showing their relevance in the modern world and piggybacking onto a publicly accepted goal of conservation that, as cynics argue, in most cases is unlikely to be reached but a good marketing strategy for the time being. I am sure that the author does not want to give the cynics more fuel for their arguments.

Further- to be ethically responsible in the promotion of ideas as this paper offers, is to understand how few projects in the model proposed in the paper have actually succeeded in practice. I take the (more modest) view of the Smithsonian which seems a genuine and achievable goal, that zoos need to learn what birds actually need in order to live and survive in the wild and that the passenger pigeons could not be saved because no-one knew how to look after them.

If these changes to the ms are made in full, I have no hesitation in recommending this paper for publication.

I have edited the start of the conclusion as suggested. The line numbers on my copy of the manuscript and that suggested by the reviewer did not match so please check that I have edited the correct section.

SOME ADDITIONAL CORRECTIONS:

Line 353/54 --- “with a final search in January 2019 for any December 2018 that may have been published”.  ”for any December 2018”??  something missing here-sentence does not make sense

Edited to include the word articles.

Line 420 —‘to provide an evidence’- drop “an”

Edited.

And in the References  

Quite a few references are incomplete short hand (as if written only to an initiated few) and need to be completed; e.g.. Refs 5,11-14 , 33, 52 -54, 79,80,82 –the most minimalist and entirely obscure entry is “EAZA. About us. 2021.”

Any such entries must be completed:

First) All abbreviations must be spelled out in full first – no CPSG, BIAZA, CBD –  may be enough for a specific in-group but the readership for the journal to which this paper has been submitted is for a wider audience - –

Second): publications of books and pamphlets and other promotional material must have a place and publisher even  when produced internally (i.e. even if authorship and publisher are the same  or, if only produced online, provide the full website details)

Third) Ref. 15 (Redondo) is obviously a thesis and it must state so (Doctoral thesis, University Exeter)—include also place and country—there are several ‘Exeter’ places in the world.  

I have edited all of the references highlighted accordingly. Please do let me know if there are any further incorrect entries. 

Round 3

Reviewer 3 Report

I know the author’s work. He was instructed to remove these lines, but he simply moved the same contents and placed it further down in the conclusion and rearranged the sentences a bit so they wouldn’t be found. My early recommendations were: if these 3 sentences are removed, I have no hesitation in recommending publication.

My suggestion is let the author simply say that,

“The corrections have not been made in full. The sentences the author was asked to remove (i. e. the first sentences in the conclusion in the original ms) have simply been shifted further down in the conclusion (now third para lines 469-475) and still require removal.”

On the other hand, please express it clearly and argue why the author does not want to consider the reviewer's suggestions.

Author Response

I'm sorry that this reviewer feels that their comments have not been actioned. 

Thank you to the editor in chief for providing clear instruction on what the required deletion was. This section of the conclusion has been removed. 

In my previous reply I explained that I was unsure as to the section that was asked being asked for removal. The conclusion was extended with more information and further examples as was requested in the developmental suggestions from the other reviewers and from the editor, and from this reviewer's comments. Hence why the information was moved around and the start of the conclusion altered. There was no burying of information, the conclusion was re-written based on the feedback provided by the paper's reviewers.

Round 4

Reviewer 3 Report

I have now read through the entire ms again and am satisfied that all indicated corrections and cuts have been made. However, having read it again there is one important omission. Under 5.1 second sentence -(now lines 402-403):

The sentence reads: "Precedent is available in the literature that shows how zoo birds can support field-based conservation." This is an important claim and really needs a reference.

Apart from this one correction, my recommendation supports this paper for publication.

Author Response

Thank you for identifying. I have added several citations to cover bird species generally and bird species specifically to show the projects that have involved zoos and captive facilities and how reintroductions and conservation work is documented in the literature. Thank you for the comments to help improve the manuscript overall.