Nature calls: intelligence and natural foraging style predict poor welfare in captive parrots

Understanding why some species thrive in captivity, while others struggle to adjust, can suggest new ways to improve animal care. Approximately half of all Psittaciformes, a highly threatened order, live in zoos, breeding centres and private homes. Here, some species are prone to behavioural and reproductive problems that raise conservation and ethical concerns. To identify risk factors, we analysed data on hatching rates in breeding centres (115 species, 10 255 pairs) and stereotypic behaviour (SB) in private homes (50 species, 1378 individuals), using phylogenetic comparative methods (PCMs). Small captive population sizes predicted low hatch rates, potentially due to genetic bottlenecks, inbreeding and low availability of compatible mates. Species naturally reliant on diets requiring substantial handling were most prone to feather-damaging behaviours (e.g. self-plucking), indicating inadequacies in the composition or presentation of feed (often highly processed). Parrot species with relatively large brains were most prone to oral and whole-body SB: the first empirical evidence that intelligence can confer poor captive welfare. Together, results suggest that more naturalistic diets would improve welfare, and that intelligent psittacines need increased cognitive stimulation. These findings should help improve captive parrot care and inspire further PCM research to understand species differences in responses to captivity.

Line 30: I read endangeredness as a threat level but this relates to the likelihood of a poor welfare problem being experienced? But then I get to line 61 and see it is related to conservation threat? Please can this be explained more carefully?
If you are discussing how threatened a species is, threat level is probably a better term than "endangeredness".
Methods are clear and repeatable and the supplementary information is useful for their understanding.
Line 97: Can you explain the key source for social behaviour?
Line 101: Please explain or define what you mean by encephalisation in this section. Is brain size a proxy for this?
Line 103: Where do captive population sizes come from?
Is aviculture defined as captive populations in managed programmes, i.e. those run by accredited or member organisation zoos? Or for private breeders too?
Line 132: I am not familiar with "leave-one-out" analysis. Can this be explained?
For all models, can you publish the final model that was run?
Line 153: I am struggling to work out why you decide to include and leave out species. What's the biological or ecological decision behind this, and the long term impact on your results?
Line 157: suggest you explain the correlated predictor here, how strong this was, and what you did. Line 189 suggest that you don't lead this paragraph with the ambiguous result. Present the clear result first, that small populations and number of breeding pairs clearly predicted hatch rates. Threat level is unclear. I don't think it is appropriate to try and draw a conclusion from the threat level data given your own explanation of how sensitive it is to specific data points.
Line 160: because the grey parrot is so common in captive populations, is this why it has such an influence? So is the small population of each individual species in this large but varied dataset causing issues with the reliability of the analysis output?
The discussion is thorough and provides a detailed evaluation of results. I would like to see more application of the findings to the actual birds that will benefit from them. Currently this is glossed over or left to the reader to infer.
Line 226-227: I find this sentence hard to follow. And please explain your reasoning for the Type II error.
Line 240-241: Please explain what you mean by better care, and provide some examples of how this can be done (based on your results). Less sunflower seeds, more environmental complexity, for example.

Recommendation
Major revision is needed (please make suggestions in comments) Scientific importance: Is the manuscript an original and important contribution to its field? Excellent General interest: Is the paper of sufficient general interest? Excellent Quality of the paper: Is the overall quality of the paper suitable? Good Is the length of the paper justified? Yes Should the paper be seen by a specialist statistical reviewer? No Do you have any concerns about statistical analyses in this paper? If so, please specify them explicitly in your report. Yes It is a condition of publication that authors make their supporting data, code and materials available -either as supplementary material or hosted in an external repository. Please rate, if applicable, the supporting data on the following criteria.

Do you have any ethical concerns with this paper? No
Comments to the Author General: Throughout the manuscript the term captive is utilized when referring to many different situations. This includes pets, aviculture, zoos, etc. and the manuscript could benefit from calling out specifically which area is being referenced when making different statements. Abstract: Line 2: "Others, however, breed poorly, or display stereotypic behaviours indicating stress." Please rephrase as not all stereotypic behavior is indicative of current stress.
Line 6: "Species with large relative brain sizes proved most at risk of oral and whole-body stereotypic behaviour: the first empirical evidence that high intelligence predicts poor captive welfare." Similar, please rephrase as not all stereotypic behavior is indicative of current poor welfare, which is phrased well in the introduction. In addition, statement is generalized, should be specific to Psittaciformes.
Introduction: Page 2 Line 4: Maybe consider a different word choice other than "dogged". Page 2 Line 8-11: These numbers are estimates, this should be more clear for the reader.

Methods:
Page 5 Line 77-79: FDB and stereotypic behaviors should be defined for the reader in the manuscript. Page 6 Line 107-10: Value that was utilized to determine significance for models should be in the methods.
Results: Page 8 Line 144: Results are either significant or they are not, results don't "tip into significance." Table 2: Trends (p&lt;0.01) should be removed, and only highlight results that are actually significant. The abstract, results and discussion will need to be updated based on this change to the manuscript. Even after removing all non-significant "trends" the results still have at least one significant predictor for each of the outcome variables. Discussion: Page 11 Line 223-25: Results don't indicate this idea, this is one possible explanation. This paragraph should be updated to reflect this difference. Page 12 Line 264: Starting at this point, this will need to be updated, most likely removed after removing all "trends" from the manuscript. Page 13 Line 285: Intelligence in Psittaciformes, but cannot generalize across all taxonomic groups.
Decision letter (RSPB-2021-1027.R0) 12-Jul-2021 I am writing to inform you that this version of your manuscript RSPB-2021-1027 entitled "Nature calls: Intelligence and natural foraging style predict poor welfare in captive parrots" has, in its current form, been rejected for publication in Proceedings B.
This action has been taken on the advice of referees, who have recommended that substantial revisions are necessary. With this in mind we would be happy to consider a resubmission, provided the comments of the referees are fully addressed. However please note that this is not a provisional acceptance.
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Please find below the comments made by the referees, not including confidential reports to the Editor, which I hope you will find useful. Please find below the comments made by the referees, not including confidential reports to the Editor, which I hope you will find useful. If you do choose to resubmit your manuscript, please upload the following: 1) A 'response to referees' document including details of how you have responded to the comments, and the adjustments you have made.
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Sincerely, Professor Gary Carvalho mailto: proceedingsb@royalsociety.org Associate Editor Board Member Comments to Author: The reviewers have provided positive feedback and constructive comments that should help to improve the manuscript -particularly in relation to the clarity in use of terminology and the appropriate presentation of the statistical outcomes.
Reviewer(s)' Comments to Author: Referee: 1 Comments to the Author(s). A useful and relevant paper that provides some clear applications to industry and the keeping of animals based on ecological knowledge. This is a well-written and well structured paper that has novel and interesting findings. It would benefit from some clarity in the explanations of terms used, the details provided in the statistical modelling and more consideration given to the application of results.
A couple of minor points for consideration: Take with statements that "this is the first to show something" as there may be evidence somewhere that could come to light in the future.
Avoid the word prove. We support or refute in scientific research.
I can see that you like the term "thrive or fail" but to me, fail does not seem the correct wording for such a statement. Species can fail to adapt to a captive population, but in this sense it is not the individual's failure to cope with its captive husbandry. The husbandry is failing the individual. The animal is not at fault. Please change this word (wherever it occurs in the manuscript).
The abstract provides some really useful explanation of the key results but the concluding statement is quite weak. Could you suggest how they are applied to parrot care? Also, suggest you remember the word "novel" (findings) because they are currently novel but the paper will age.
The introduction is clear and well explained. Is the word "dogged" correct (line 4)? Something more scientific and less colloquial sounds more appropriate.
The size of the captive parrot population seems huge. How measured? Is this including the budgerigar? And is this an estimation for the entire order?
Species comparison for the grey parrot could be helpful (line 22). Line 30: I read endangeredness as a threat level but this relates to the likelihood of a poor welfare problem being experienced? But then I get to line 61 and see it is related to conservation threat? Please can this be explained more carefully?
If you are discussing how threatened a species is, threat level is probably a better term than "endangeredness".
Methods are clear and repeatable and the supplementary information is useful for their understanding.
Line 97: Can you explain the key source for social behaviour?
Line 101: Please explain or define what you mean by encephalisation in this section. Is brain size a proxy for this?
Line 103: Where do captive population sizes come from?
Is aviculture defined as captive populations in managed programmes, i.e. those run by accredited or member organisation zoos? Or for private breeders too?
Line 132: I am not familiar with "leave-one-out" analysis. Can this be explained?
For all models, can you publish the final model that was run?
Line 153: I am struggling to work out why you decide to include and leave out species. What's the biological or ecological decision behind this, and the long term impact on your results?
Line 157: suggest you explain the correlated predictor here, how strong this was, and what you did. Line 189 suggest that you don't lead this paragraph with the ambiguous result. Present the clear result first, that small populations and number of breeding pairs clearly predicted hatch rates. Threat level is unclear. I don't think it is appropriate to try and draw a conclusion from the threat level data given your own explanation of how sensitive it is to specific data points.
Line 160: because the grey parrot is so common in captive populations, is this why it has such an influence? So is the small population of each individual species in this large but varied dataset causing issues with the reliability of the analysis output?
The discussion is thorough and provides a detailed evaluation of results. I would like to see more application of the findings to the actual birds that will benefit from them. Currently this is glossed over or left to the reader to infer.
Line 226-227: I find this sentence hard to follow. And please explain your reasoning for the Type II error. Line 291: Why should PCM be used more? Could you add context to the end of your conclusion?
Referee: 2 Comments to the Author(s). General: Throughout the manuscript the term captive is utilized when referring to many different situations. This includes pets, aviculture, zoos, etc. and the manuscript could benefit from calling out specifically which area is being referenced when making different statements.
Abstract: Line 2: "Others, however, breed poorly, or display stereotypic behaviours indicating stress." Please rephrase as not all stereotypic behavior is indicative of current stress.
Line 6: "Species with large relative brain sizes proved most at risk of oral and whole-body stereotypic behaviour: the first empirical evidence that high intelligence predicts poor captive welfare." Similar, please rephrase as not all stereotypic behavior is indicative of current poor welfare, which is phrased well in the introduction. In addition, statement is generalized, should be specific to Psittaciformes.
Introduction: Page 2 Line 4: Maybe consider a different word choice other than "dogged". Page 2 Line 8-11: These numbers are estimates, this should be more clear for the reader.

Methods:
Page 5 Line 77-79: FDB and stereotypic behaviors should be defined for the reader in the manuscript. Page 6 Line 107-10: Value that was utilized to determine significance for models should be in the methods.
Results: Page 8 Line 144: Results are either significant or they are not, results don't "tip into significance." Table 2: Trends (p<0.01) should be removed, and only highlight results that are actually significant. The abstract, results and discussion will need to be updated based on this change to the manuscript. Even after removing all non-significant "trends" the results still have at least one significant predictor for each of the outcome variables. Discussion: Page 11 Line 223-25: Results don't indicate this idea, this is one possible explanation. This paragraph should be updated to reflect this difference. Page 12 Line 264: Starting at this point, this will need to be updated, most likely removed after removing all "trends" from the manuscript. Page 13 Line 285: Intelligence in Psittaciformes, but cannot generalize across all taxonomic groups.

Do you have any ethical concerns with this paper? No
Comments to the Author This is a useful and interesting paper that has been improved and clarified following the first review. The authors have provided useful details to expand on specific areas of the study. All reviewer comments have been answered and suitable extra discussion and evaluation have been provided where relevant. I am happy to approve this paper for publication.

06-Sep-2021
Dear Professor Mason I am pleased to inform you that your Review manuscript RSPB-2021-1952 entitled "Nature calls: Intelligence and natural foraging style predict poor welfare in captive parrots" has been accepted for publication in Proceedings B.
The referee(s) do not recommend any further changes. Therefore, please proof-read your manuscript carefully and upload your final files for publication. Because the schedule for publication is very tight, it is a condition of publication that you submit the revised version of your manuscript within 7 days. If you do not think you will be able to meet this date please let me know immediately.
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Sincerely, Professor Gary Carvalho mailto:proceedingsb@royalsociety.org Reviewer(s)' Comments to Author: Referee: 1 Comments to the Author(s). This is a useful and interesting paper that has been improved and clarified following the first review. The authors have provided useful details to expand on specific areas of the study. All reviewer comments have been answered and suitable extra discussion and evaluation have been provided where relevant. I am happy to approve this paper for publication.

08-Sep-2021
Dear Professor Mason I am pleased to inform you that your manuscript entitled "Nature calls: Intelligence and natural foraging style predict poor welfare in captive parrots" has been accepted for publication in Proceedings B.
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Ref 1
Comments to the Author(s). A useful and relevant paper that provides some clear applications to industry and the keeping of animals based on ecological knowledge. This is a well-written and well structured paper that has novel and interesting findings.

Many thanks for your nice comments here (and the constructive ones throughout).
It would benefit from some clarity in the explanations of terms used, the details provided in the statistical modelling and more consideration given to the application of results.

Your suggestions were very helpful, and we hope we've complied with them as you envisaged.
A couple of minor points for consideration: Take with statements that "this is the first to show something" as there may be evidence somewhere that could come to light in the future.
Very true --though we are certain that to date, there has been no empirical evidence that intelligence can put species at risk of poor welfare.
Avoid the word prove. We support or refute in scientific research.
Totally agree; in the abstract we were using it in the non-scientific sense of "to demonstrate" or "to show" (to save words), but can now see that this is needlessly confusing. Text is now changed accordingly to "were most prone to".
I can see that you like the term "thrive or fail" but to me, fail does not seem the correct wording for such a statement. Species can fail to adapt to a captive population, but in this sense it is not the individual's failure to cope with its captive husbandry. The husbandry is failing the individual. The animal is not at fault. Please change this word (wherever it occurs in the manuscript).
Totally agree with your sentiment here. If we accidentally implied that animals are at fault, that is bad: thankyou for pointing this out. In the abstract, we removed that clause (saving words: nice as the limit is 200). And in line 1 of the Introduction, we replaced "fail" with "struggle", as we also did in the very last line of the paper.
The abstract provides some really useful explanation of the key results but the concluding statement is quite weak. Could you suggest how they are applied to parrot care?
We reordered it so that the penultimate sentence emphasises parrot husbandry more ("Together, results suggest that more naturalistic diets would improve welfare and intelligent psittacines need increased cognitive stimulation."), but we are very constrained by the word limit (200 words!). We also do want to highlight the future value of PCMs (the last line), as the application of this ecological/evolutionary method to welfare issues is still very new and with great untapped potential.
Also, suggest you remember the word "novel" (findings) because they are currently novel but the paper will age.

Good point; removed
The introduction is clear and well explained.

Thankyou!
Is the word "dogged" correct (line 4)? Something more scientific and less colloquial sounds more appropriate.
It's a bit poetic, you're right. Changed to "prone to" (new line 6).
The size of the captive parrot population seems huge. How measured? Is this including the budgerigar? And is this an estimation for the entire order?
It is estimated by Jamie Gilardi, director of the World Parrot Trust. We believe it does include budgerigars. We are hitting the page limit for this journal so are unable to add too many details, but we augmented the text to add (the underlining indicating new text): "Phylogenetic comparative methods (PCMs) developed by evolutionary biologists can reveal why species show such variation. These allow multi-species datasets to be statistically analysed to identify attributes that predispose certain taxa to problems in captivity, while controlling for similarities arising from evolutionary relatedness" (New lines 27-30). We also added your suggested figure to the Supported Materials (new Fig S1), with some explanatory text: nice idea so thank you.

At lines 302-303, we also say "PCMs -with their abilities to interrogate multi-species datasets and address hypotheses that would otherwise be challenging to test".
Line 30: I read endangeredness as a threat level but this relates to the likelihood of a poor welfare problem being experienced? But then I get to line 61 and see it is related to conservation threat? Please can this be explained more carefully? If you are discussing how threatened a species is, threat level is probably a better term than "endangeredness".
Threat level is one of the variables we use to test this hypothesis, so we want to stick to "endangeredness" for the broader concept. But we do see it could be worded more clearly, so thanks for pointing this out. Lines and at risk of stress when captive [2, 32]. Furthermore, the small population sizes of rare species can cause further issues".

Lines 109-110 also now say: "Our two measures of endangeredness were threat level according to IUCN Red List categories, and ex situ rarity"
Line 47: Perhaps explain boredom?
Ormrod and Morris (who we cite here), were using this term rather colloquially so we left as is here (plus we don't want to make this long section longer). But we now define the term at new lines 250-251, where a precise meaning is important: "promoting boredom (aversive states caused by monotony [38])" Methods are clear and repeatable and the supplementary information is useful for their understanding.
Thankyou! We've also added a bit more detail to the Supplement to make it more useful still (new Fig S1; plus in Section 6, details of how to access species-typical data from two online datasets).
Line 97: Can you explain the key source for social behaviour? Table 1

Both [70] and [71] contained data on feeding groups, and [71] also had data on roosting group sizes.
Line 101: Please explain or define what you mean by encephalisation in this section. Is brain size a proxy for this? Relative brain size (i.e. brain size corrected for allometric effects of body size). This is now defined on new line 54 (and was also in Table 1, and is still there).
Line 103: Where do captive population sizes come from?
They come from the aviculture dataset (see Table 2); thus from the private breeders who hold the vast majority of breeding parrots.
Is aviculture defined as captive populations in managed programmes, i.e. those run by accredited or member organisation zoos? Or for private breeders too?
No, aviculture means breeding centres, which are private. Zoo populations are small, and hardly any parrots in zoos are managed using studbooks (under a dozen species).
For clarity on this, at lines 76, 101, and 111 we have now changed "aviculture" to "private breeding centres".
Line 132: I am not familiar with "leave-one-out" analysis. Can this be explained?

New lines 142-147 now say (new bits being underlined): "To assess whether any significant findings merely reflected outliers, we used a custom version of the influ_phylm function within the 'sensiPhy' package [102]. This performs "leave-one-out" deletion analyses (removing each species in turn and recalculating the intercept, slope and corresponding p value for each parameter), a species being deemed 'influential' if its removal yielded a standardised difference >2. This revealed whether any results critically relied on the influence of just one or two particular datapoints".
For all models, can you publish the final model that was run?
Throughout the manuscript and supplementary material, we have followed the principle that anyone should be able to replicate our methods (including all the decisions that led to the final models). Thus our methods are very transparent and replicable, and the final models and their rationales are all summarised in Table S6. Furthermore, the R scripts are provided in the relevant Dryad repository (see Section 6 of the Supporting Material), where the full dataset itself is also freely available to anyone wanting to check our analyses. (Note that it's possible Dryad may not make this link active until the paper is in press, however)