Re-Assessing the Importance of Evidence-Based Inputs for Positive Zoo and Aquarium Animal Welfare Outputs

Round 1
Reviewer 1 Report
Comments and Suggestions for AuthorsAuthors characterized the efficacy of having species-specific input-based measures of animal welfare as part of a holistic animal care program, and how inputs can inform and be informed by housing, husbandry, and welfare. Therefore, the ideas and intention are important to understanding animal welfare and its assessments which are varied, multimodal, species specific, and therefore necessitates further works like this.
Overall, the manuscript is well written however there are several punctuation and keystroke errors present. I recommend a thorough editing prior to publication. Authors clearly and succinctly outline their thesis and justifications, and most figures further illustrate their arguments. Though I do not fully agree with the premise, I have no arguments against its publication. That said, one considerable aspect missing is scale – authors not note how inputs should be evaluated outside the presence or absence of an intended (or unintended) outcome. Is a dyadic assessment enough to determine efficacy of an input, or are more robust measures of outcomes (% time in activities, patterns of positive change, return to baseline when removed, etc) needed? I assume the latter, but do not believe that is clearly stated within the manuscript. Authors note that caretakers need to ascertain if inputs provided meet an animal’s core needs and opportunity, but are limited in describing how this may occur.
My comments are summarized below.
Ln 20-21: unsure how the size of a zoo correlates to the use of outputs and nature of inputs. Consider revising to be more general or possibly focusing on accreditation bodies. Likewise, I do not believe this is addressed in the body of the manuscript.
Ln 31. Is the statement "...outputs can never be positive" true? I recognize authors are likely being provocative, but please consider revising.
Ln 129-130. Should indicators be validated and replicable within species, e.g., "...across individuals within a species and zoos"?
Lns 142-143. This is a good list of realistic limitations. Recommend adding the time investment in conducting observations and skills required for even simple analysis as one of the limitations of behavioral data collection. There is ample evidence showing keepers report 'lack of time' as a primary limitation to their conducting behavior evaluation. Likewise, understanding which inputs are most effective in eliciting meaningful outputs requires evaluation, therefore investment in that time can produce such efficiencies, which aligns to your thesis.
Lns 217-218. As written, "including farm and laboratory animals" reads as if that is a further definition of the prior "for several species", which I believe is not intended. Recommend revising, e.g., "...important for several species - including animals living in farm and laboratory environments - are likely..." to reinforce the 'species and environment' focus of this section.
Lns 218-219. I understand where this is going, but worry that concluding with the statement "welfare of all zoo-kept animals" is too broad and likely species-biased. There are species cared for in zoos in which this would not be true and likewise contradicts Section 3.2 below. Please consider revising.
Fig 2. This is a helpful figure - thank you. Should the first question, "What would you like the animal to do" be from the animal/species' perspective and not from a human/caregiver's? E.g., "what should the animal be doing" or " what behavior should the animal be exhibiting?". Consider revising.
Fig 3. Is this figure necessary? Text seems sufficient.
Lns 340-343. This sentence is awkward - please revise.
Author Response
Replies to reviewers
Reviewer 1
Authors characterized the efficacy of having species-specific input-based measures of animal welfare as part of a holistic animal care program, and how inputs can inform and be informed by housing, husbandry, and welfare. Therefore, the ideas and intention are important to understanding animal welfare and its assessments which are varied, multimodal, species specific, and therefore necessitates further works like this. Overall, the manuscript is well written however there are several punctuation and keystroke errors present. I recommend a thorough editing prior to publication. Authors clearly and succinctly outline their thesis and justifications, and most figures further illustrate their arguments. Though I do not fully agree with the premise, I have no arguments against its publication. That said, one considerable aspect missing is scale – authors not note how inputs should be evaluated outside the presence or absence of an intended (or unintended) outcome. Is a dyadic assessment enough to determine efficacy of an input, or are more robust measures of outcomes (% time in activities, patterns of positive change, return to baseline when removed, etc) needed? I assume the latter, but do not believe that is clearly stated within the manuscript. Authors note that caretakers need to ascertain if inputs provided meet an animal’s core needs and opportunity, but are limited in describing how this may occur.
Thank you for the feedback and positive comments. We have attempted to address your concerns and comments around how to evaluate inputs and how to meet a species’ core needs at the start of section 3. We have included information on the need for robust measures and how such measures are fed back to be used by animal care staff to support provision of appropriate husbandry.
My comments are summarized below.
Ln 20-21: unsure how the size of a zoo correlates to the use of outputs and nature of inputs. Consider revising to be more general or possibly focusing on accreditation bodies. Likewise, I do not believe this is addressed in the body of the manuscript.
Thank you for the comment. We are not discussing the size of the zoo here, we mean the large zoo organisations such as AZA, EAZA, WAZA, etc. We have included “membership” in the abstract.
Ln 31. Is the statement "...outputs can never be positive" true? I recognize authors are likely being provocative, but please consider revising.
Thank you for the comment. We have amended this to state truly or meaningfully positive. However, we do not wish to remove this because if care is not correct, a zoo-housed species will not experience positive welfare.
Ln 129-130. Should indicators be validated and replicable within species, e.g., "...across individuals within a species and zoos"?
Thank you for the feedback. We have edited this to state within individuals and across zoos.
Lns 142-143. This is a good list of realistic limitations. Recommend adding the time investment in conducting observations and skills required for even simple analysis as one of the limitations of behavioral data collection. There is ample evidence showing keepers report 'lack of time' as a primary limitation to their conducting behavior evaluation. Likewise, understanding which inputs are most effective in eliciting meaningful outputs requires evaluation, therefore investment in that time can produce such efficiencies, which aligns to your thesis.
Thank you for the positive feedback here. We have included your suggested addition with new references to support the examples you have kindly provided.
Lns 217-218. As written, "including farm and laboratory animals" reads as if that is a further definition of the prior "for several species", which I believe is not intended. Recommend revising, e.g., "...important for several species - including animals living in farm and laboratory environments - are likely..." to reinforce the 'species and environment' focus of this section.
Thank you for the suggestion. We have amended this accordingly including your revision to the text.
Lns 218-219. I understand where this is going, but worry that concluding with the statement "welfare of all zoo-kept animals" is too broad and likely species-biased. There are species cared for in zoos in which this would not be true and likewise contradicts Section 3.2 below. Please consider revising.
Thank you for the suggestion. We have removed the word “all” from this statement and we have edited to suggest for some species in some situations.
Fig 2. This is a helpful figure - thank you. Should the first question, "What would you like the animal to do" be from the animal/species' perspective and not from a human/caregiver's? E.g., "what should the animal be doing" or " what behavior should the animal be exhibiting?". Consider revising.
This is a great point. Thank you for clarifying and we have edited the figure according to this suggestion.
Fig 3. Is this figure necessary? Text seems sufficient.
Thank you for the feedback. We have deleted this figure and amended the text to improve the discussion of this point shown by the figure.
Lns 340-343. This sentence is awkward - please revise.
Thank you for the feedback. We have edited this sentence to improve clarity by changing the wording and focus of the argument.
Reviewer 2 Report
Comments and Suggestions for AuthorsGeneral comments
While the article presents a valuable foundation for discussing animal welfare in zoological institutions, it does not yet meet the standards expected of a comprehensive review. Many key concepts are introduced but only superficially explored, resulting in a broad overview rather than an in-depth, critical analysis. As a result, the manuscript lacks the depth and nuance necessary to make a substantial scientific contribution.
The reference list is notably limited and does not reflect the breadth of current literature available on the topic. A more robust integration of recent, peer-reviewed studies would significantly enhance the contextualization, credibility, and originality of the arguments presented. Furthermore, the manuscript would benefit greatly from the inclusion of concrete examples, measurable indicators, and comparative analyses of different approaches to animal welfare in zoos. These additions would improve both the academic rigor and the practical relevance of the article. (see attached document)
Comments for author File: Comments.pdf
Author Response
Thank you for the comments and feedback. Both authors have read over them thoroughly and we have had a meeting to discuss. We have really struggled to understand what we are addressing and how to action the suggested edits. The premise of this paper is to evaluate and explain the importance of evidence-based inputs to zoo animal husbandry, as these evidence-based inputs form the basis of positive animal welfare outputs. The reviewer has suggested including information on conservation, reintroduction and social structure. We feel these are are not core themes of the paper and we ask for editorial support from the editors as to how best to respond to this review. We have attempted to respond to comments but we have been left very confused by this review.
Reviewer 2
General comments
While the article presents a valuable foundation for discussing animal welfare in zoological institutions, it does not yet meet the standards expected of a comprehensive review. Many key concepts are introduced but only superficially explored, resulting in a broad overview rather than an in-depth, critical analysis. As a result, the manuscript lacks the depth and nuance necessary to make a substantial scientific contribution.
The reference list is notably limited and does not reflect the breadth of current literature available on the topic. A more robust integration of recent, peer-reviewed studies would significantly enhance the contextualization, credibility, and originality of the arguments presented. Furthermore, the manuscript would benefit greatly from the inclusion of concrete examples, measurable indicators, and comparative analyses of different approaches to animal welfare in zoos. These additions would improve both the academic rigor and the practical relevance of the article.
Thank you for the feedback. Based on our responses to all reviewers, we have expanded the number of references included and provided further examples and citations. Please note that we were not providing a systematic review of the welfare literature, but rather our perspective on the needs of species-specific, evidence based inputs as an important support for positive welfare outputs. We hope our revisions have strengthened these ideas.
Integration of Existing Bibliography and Cite concrete Examples of Practices Applied in Zoos to Improve Animal Welfare
Cite and add in the text specific studies that bolster the concepts presented, such as those addressing the importance of environmental enrichment, the connection between natural behaviors and the psychological well-being of animals, and the scientific evidence regarding biological responses to stress. For instance, references to recent research on the use of cortisol as an indicator of stress, or studies on changes in natural behaviors in suboptimal environments.
- Thank you for the feedback. We believe that we have included further sources, based on our responses to all reviewer queries, and we have extended the context of our arguments and narrative throughout the paper. We have almost doubled the use of examples in the paper. We believe that we have added clarity and focus accordingly, and we hope that these cumulative corrections address your concerns above. We have also changed the type of paper from review commentary to better reflect that this is a concept piece.
Compare Different Approaches: discuss more thoroughly the existing alternatives to proactive approaches and cite concrete examples of practices applied in zoos to improve animal welfare
Thank you for the comment, however we are unsure as to what the reviewer means here. We are not sure why we would want to argue against proactive responses to promoting zoo animal welfare. We certainly do not wish to include examples of how we should simply “firefight” existing issues, but rather our paper aims to show why we need to build evidence in all aspects of zoo and aquarium housing and husbandry. If the reviewer can provide more clear, specific instruction on what elements of the paper could be improved, we would be happy to action.
Expand the Discussion on the Integration Between Zoos and Nature Reserves: the discussion on the role of zoos in broader conservation strategies is underdeveloped. The article mentions several tools and research documents that could be enhanced by incorporating examples of practical approaches or more recent studies on specific species. Include recent research on reintroduction programs and welfare-driven conservation strategies.
- Thank you for the feedback here but, respectfully, we decline to address this because our paper is not about nature reserves, nor is it about reintroduction programmes. Our paper centres on inputs for animals in zoos and aquariums and how these should be evidenced based. We are not discussing the role of individual animals in reintroduction biology, which we feel is a very large topic and one that will have its own suite of literature to focus on.
Improve application of Scientific Research in Daily Zoo Management. While the article acknowledges the importance of evidence-based research, it does not provide a detailed examination of how scientific findings can be effectively integrated into the daily management practices of animals in zoos and aquariums. There is limited discussion on how keepers, researchers, and facility managers can collaborate to translate scientific insights into routine husbandry protocols.
Thank you for the feedback. We have included a paragraph (lines 403-418) suggesting how relevant welfare inputs can be further identified using a science-based approach to support our paper’s overall aim of using evidence to advance care.
A stronger focus on the mechanisms through which zoological institutions can integrate scientific research in their day-to-day operations would enhance the article's practical relevance. For instance, the discussion could be expanded to include examples of ongoing professional development programs for zoo personnel, active participation of animal care staff in data collection and behavioral monitoring, and the positive impact of such integrative practices on animal welfare outcomes. Emphasizing the value of cross-disciplinary collaboration could further reinforce the role of science as a cornerstone of modern zoological management.
See our previous comment on the use of scientific data. This is a key focus of the paper and in our concluding statements, and in Table 1, we call for these approaches advocated by the reviewer. If there are specific areas that need to be further developed, please can these be highlighted to us for reflection and potential revision.
Enhanced Discussion on the Integration of Conservation Efforts: while the article briefly addresses the role of zoos in species conservation, it does not fully examine the interdependency between animal welfare and conservation outcomes. A more comprehensive exploration could include:
- An analysis of how animal welfare research contributes to achieving conservation objectives. Recent studies exploring the success of conservation programs, where human intervention and environmental management are aligned with positive species outcomes, would be valuable to incorporate.
- A more detailed discussion on welfare-oriented conservation strategies, such as captive breeding programs that enhance animal welfare to support successful reintroduction into natural habitats."
Highlights
- Add references on Social Well-being and Group Dynamics (line 165-181)
Although the article discusses both physical and psychological welfare, the social dimension is only briefly mentioned. Social well-being—particularly for gregarious species—deserves more in-depth treatment, as do the social interactions both among animals and between animals and their keepers.
Areas for Improvement:
- A more thorough analysis of social dynamics in captivity is recommended, particularly focusing on how enclosure design and management policies can promote the development of positive social bonds. The inclusion of additional examples illustrating how socialization and the presence of conspecifics influence animal welfare would significantly strengthen the discussion.
- The effects of enrichment or environmental interventions on health and welfare and the variability linked to individual differences in personality. Moreover, the influence exerted by group members on one another is shaped by the group’s composition, as well as by the individual characteristics and temperaments of its members. These factors can affect how animals interact with their surroundings and influence the expression of certain behaviors
- Add references in Analysis of Psychological Well-Being (line 191-223) Although the important role of positive emotions such as joy and curiosity for animal well-being is mentioned, there is a lack of a thorough analysis of animal psychology in relation to quality of life in captivity.
Thank you for the feedback. We have a strong thread of including information on psychological welfare (animal-based outputs) throughout this manuscript. We have included Qualitative Behaviour Assessment, for example, as a mean of inferring mood and emotion that is developing traction in zoos. We are unsure of the need to focus on social dynamics as we talk at length about behaviour, and behavioural needs, therefore, social behaviour is part of this element of consideration.
Areas for Improvement:
- Add in the text more recent research on animal cognition that demonstrates animals' emotional awareness and the connection between environmental management and mental well-being.
The effect of environment stimuli, resources, and learning opportunities that shape cognitive and behavioral strategies, and how social interactions facilitate the acquisition of skills through observation, cooperation, and social learning
- Improve citation and add in the text recent studies on the importance of individual personality traits, life history, and social housing conditions—such as whether animals are housed alone or in groups—in relation to their species-specific sociality. Although the article correctly critiques the limitations of a “one-size-fits-all” approach to animal welfare, it does not sufficiently elaborate on how species-specific and individual-specific needs can be systematically assessed and addressed within captive management practices. In particular, the complex interplay between genetic variability and individual behavioral differences within the same species remains underexplored. A more comprehensive discussion of tailored welfare strategies that account for such intra- and interspecific variation would significantly enhance the article’s depth and applicability.
Thank you for the comment. We have rationalised the title of the manuscript, and expanded on the papers aims and overall themes. We hope this clarifies the rationale of the manuscript.
- Cite and add references in the text on pratical enrichment projects (line 225-235) Although the importance of environmental enrichment is emphasized, the article could benefit from the inclusion of more practical examples and go deeper also on cognitive enrichment." -
- Include case studies or pilot projects demonstrating the application of enrichment protocols.
- In controlled environments, species management requires the implementation of targeted strategies aimed at ensuring animal welfare, the expression of natural behaviors, and an optimal psychophysical state.
- Among the various forms of enrichment, cognitive enrichment has proven particularly effective—not only because it presents animals with new challenges that reduce boredom and foster the development of mental abilities, but also because it plays a significant role in promoting animal well-being
- Integrating research and management practices for wildlife conservation in zoos. (e.g D'Cruze, N., & MacDonald, D. W. (2018). "Bridging the gap between science and practice in zoo animal welfare." Zoo Biology, 37(1), 72-83.
Thank you for the feedback. We have provided multiple examples of different forms of enrichment, including cognitive challenge and providing enrichment that is goal orientated. We are confused as to how to best respond to these points without changing the focus of our paper, especially because we have a table that focuses on practical outputs already.
- Improve citation on Environmental and Management Effects (line 285-324) Cite how optimal conditions for animal welfare involve enabling individuals to express the full range of species-typical behaviors. By meeting psychological needs, physical health and the expression of natural behaviors can also be supported. Within this framework, providing animals in controlled environments with the opportunity to exert some degree of control over their surroundings—such as through offering choices—represents an effective mechanism for enhancing psychological wellbeing (e.g. Englund & Cronin, 2023 and many other previous research).
- Thank you for the comment. We have included references on control and choice throughout the manuscript. However, we have included the suggested reference above as well. The main premise of our paper, please see vast areas of section 2, focusses on animal behaviour outputs.
Reviewer 3 Report
Comments and Suggestions for AuthorsThe manuscript presents an argument around the prioritisation of input and output factors when assessing animal welfare in the context of zoos. The authors have made a commendable attempt to concretise the complexity of animal welfare management in a context which encompasses considerable variation from many contributing aspects, including species diversity, environmental diversity and management and husbandry diversity. The manuscript contains a few typos which can easily be addressed with a proof-read but otherwise is understandable.
Despite this, the primary issue that stands out is that the message that is being presented is not clear and coherent. Much of the text feels fragmented and the ideas presented in the manuscript do not flow from one to the other in a clear and easily-followed manner. Perhaps what is missing is a well-defined aim statement based on the existing literature and with a clear rationale to guide both the authors and the reader through the text and against which statements or sections of the text could be compared. It would also allow the authors to expand the topics covered in this manuscript, exploring them in more depth and with examples to illustrate their points, both of which are currently lacking in the manuscript. There are also some points where the authors suggest notions which are directly contradicted by the existing literature or make statements which are too broad to be upheld in context. These should be crystalised and refined so as to withstand scrutiny.
The use of figures in the manuscript is not advisable in its current form. Figure 1 seems to present an incomplete model, which could also use refinement (see Mellor et al. 2020. Animals. 10, 1870 for example). Figures 2 and 3 do not seem to fit well in the context of the text and do not provide a clear and easily-interpretable pair of models/frameworks with application potential. These too should be refined. Figure 3 in particular does not seem to add more to the manuscript than could be encompassed in one or two additional sentences.
Specific feedback is provided to the authors but generally speaking, the main issue with the manuscript is that it lacks coherence and clarity. The manuscript requires refinement and synthesis before it will be ready for publication.
Comments for author File: Comments.pdf
The English is fine but the text requires proof-reading and editing.
Author Response
Reviewer 3
The manuscript presents an argument around the prioritisation of input and output factors when assessing animal welfare in the context of zoos. The authors have made a commendable attempt to concretise the complexity of animal welfare management in a context which encompasses considerable variation from many contributing aspects, including species diversity, environmental diversity and management and husbandry diversity. The manuscript contains a few typos which can easily be addressed with a proof-read but otherwise is understandable.
Thank you for the feedback and the useful comments on our paper. We appreciate the effort in helping to develop the manuscript.
Despite this, the primary issue that stands out is that the message that is being presented is not clear and coherent. Much of the text feels fragmented and the ideas presented in the manuscript do not flow from one to the other in a clear and easily-followed manner. Perhaps what is missing is a well-defined aim statement based on the existing literature and with a clear rationale to guide both the authors and the reader through the text and against which statements or sections of the text could be compared. It would also allow the authors to expand the topics covered in this manuscript, exploring them in more depth and with examples to illustrate their points, both of which are currently lacking in the manuscript. There are also some points where the authors suggest notions which are directly contradicted by the existing literature or make statements which are too broad to be upheld in context. These should be crystalised and refined so as to withstand scrutiny.
Thank you for the feedback. We are sorry to hear that you find out paper not clear or coherent. We have stated a key aim of paper at the end of section 1, and we have since split the introduction to provide a new section (1.1.) to show our background coverage of important elements of what zoo and aquarium welfare “is all about”. We have edited the headings and subheadings of the manuscript to improve their message, and we have expanded on the key concepts covered in the article to ensure our aims are understandable. We hope that this provides more structure and clarity to our paper.
We have edited the use of references and examples throughout the manuscript, and this has provided more depth to our critique. We have almost doubled the number of references used in the manuscript. We are not seeking to provide a new model of “what welfare is”, but rather a commentary on the importance of appropriate, meaningful inputs to support a zoo animal’s chances of thus experiencing positive welfare outputs. As a result, we have edited the type of paper from review to commentary.
The use of figures in the manuscript is not advisable in its current form. Figure 1 seems to present an incomplete model, which could also use refinement (see Mellor et al. 2020. Animals. 10, 1870 for example). Figures 2 and 3 do not seem to fit well in the context of the text and do not provide a clear and easily-interpretable pair of models/frameworks with application potential. These too should be refined. Figure 3 in particular does not seem to add more to the manuscript than could be encompassed in one or two additional sentences.
Thank you for the feedback. Figure 1 is not a model designed to replace frameworks such as the Five Domains model, it is simply describing how welfare is made up of physical, behavioural and psychological components and gives examples of what these components can be. Based on feedback from other reviews, who were positive about the figure, we have strengthened the context and explanation of this figure in the text and we hope that this shows more clearly that we are providing examples of the physical, behavioural and psychological elements of welfare.
Figure 3 has since been deleted as this could more easily be explained in the text.
Figure 2 has received suggested edits from other reviewers, but the value of the figure in explaining how to provide enrichment inputs in a meaningful and goal-orientated way has been noted and therefore we believe that it supports our points in explaining how inputs (i.e., appropriate enrichment) lead to positive life experiences, the promotion of species typical behaviour patterns and positive welfare outputs.
Specific feedback is provided to the authors but generally speaking, the main issue with the manuscript is that it lacks coherence and clarity. The manuscript requires refinement and synthesis before it will be ready for publication.
We hope that our cumulative responses across reviewers have provided this enhanced discussion and analysis of our key arguments and areas of interrogation. Thank you for taking the time to provide such a thorough and useful review of our paper.
Title
The title does not appear to convey the primary message of the manuscript and should be changed. The term baseline implies data collected prior to an intervention but this is not what is being discussed. The focus of the manuscript rather seems to be on the role of environmental factors in influencing the welfare outputs of animals in a zoo context – the title should reflect this.
Thank you for the feedback. We have amended the title accordingly to “Re-assessing the importance of evidence-based inputs for positive zoo and aquarium animal welfare”
Zoo animal welfare assessment: the relevance of input-based measures
Page 3
Line 116 Here and throughout, the use of the term 'indicator' when referring to welfare-affecting inputs seems inappropriate. Indicator implies that whatever is being referenced is a signal of an outcome, something which is not necessarily always true. A specific temperature, for example, is not necessarily an indicator. In and of itself it has no relevance to welfare, unless it has a system to interact with, such as a lizard for example. Thus, it only becomes an indicator once it is coupled with an outcome which can be directly linked to welfare (e.g. behavioural thermoregulation). Being told that a lizard is living in an exhibit at 25°C does not tell you anything about its wellbeing unless more information is provided. Further to this, the role of an 'indicator' as described here will be context-specific. A large exhibit space may be meaningful for a giraffe but be of relatively less importance for a hedgehog. Thus, it can only really be interpreted as an 'indicator' once it has been assigned a context and associated with an outcome. It seems like the term itself introduces too much variation and nuance to justify its use here. Perhaps 'factor' would be a better term to use.
Thank you for the feedback and considered review of terminology here. We have checked use of the word “indicator” throughout the manuscript and provided context where required and/or changed our description. We have also reviewed the literature to check our explanation of animal-based and resource-based welfare indicators and provided new references where needed.
3.1. The importance of correct inputs
Page 5
Lines 215-219 This approach, as stated here, seems very broad and of limited application value. Presumably the authors mean that behaviours if importance across several species of similar phylogenetic or ecological contexts be assumed to be relevant to one another. One cannot reasonably argue that based on the majority of captive animals, the most predominant behaviours should be viewed as highly important for welfare, regardless of context. With this logic, dust-bathing might be considered as one of the most important behaviours and should be ensured for all animals because chickens, as one of the most abundant captive animals, benefit from being able to perform this behaviour. Trying to generate dust-bathing behaviour in captive dolphins is unlikely to generate positive welfare outcomes however, highlighting the problem with the presented approach. Perhaps this should be reworded to clarify the breadth of scope of what is being suggested.
Thank you for the comment. This section has been edited based on other reviewer feedback to clarify these points (made above). We hope that the suggested wording that we were provided with, and have integrated into the edit, cover this amendment.
Page 6
Lines 227-230 In principle, yes, this is true but there is evidence in the literature that enrichment effects are not as predictable. Applying similar enrichment across different species, even related species, does not guarantee the same outcome. For example, see Costa, R.; Sousa, C.; Llorente, M. Assessment of environmental enrichment for different primate species under low budget: A case study. J. Appl. Anim. Welf. Sci. 2018, 21, 185–199.
Thank you for the feedback and suggested citation that we have incorporated into this section of the manuscript. We have edited the discussion to ensure that measurement and assessment of individual interactions with enrichment is considered.
- Future directions for improving welfare evidence
Page 9
Line 343 What is an 'evergreen mammalian species'? The intended meaning here is not clear.
Thank you for the feedback. We have removed this term and replaced with popular/familiar.
Figures and Tables
Figure 1 The model of welfare being presented here seems incomplete. The physical attributes list here should be split into animal-centric attributes and environmental-centric attributes. The two should not be combined as the mechanisms and the modes of control around these are very different. In the context of welfare these differences have a considerable influence on how they relate to welfare state.
Thank you for the feedback. We are not attempting any new modelling animal welfare, we are just stating that welfare comprises of physical, behavioural and psychological components. However, we have amended the figure accordingly to split the physical examples into animal and environmental.
Reviewer 4 Report
Comments and Suggestions for AuthorsRe-assessing welfare priorities in the zoo: ensuring a sound baseline for meaningful welfare outputs
Manuscript ID: jzbg-3577428
Summary
This manuscript examines the current state of welfare priorities in zoos. By assessing the limitations of current welfare practices and identifying potential areas for improvement, this research aims to establish a sound baseline for meaningful welfare outputs, focusing on both the physical and psychological well-being of zoo animals.
General concept comments
Article
This manuscript addresses a crucial issue in zoo animal welfare: the balance between input- and output-based indicators, and the need for evidence-based systems that take into account the complexity of welfare assessment. However, certain stylistic and structural refinements are required to bring it to publication-ready status.
Review
Specific comments
14-17. "This paper examines the current state of welfare priorities in Zoos...". The repetition of the words 'welfare' and 'zoos' reduces the stylistic elegance. Reword: “This paper re-evaluates current welfare frameworks in zoological institutions, advocating for…”.
17-20. To improve clarity and reinforce the problem being addressed, suggest adding 1-2 examples of these limitations here.
20-23. This could benefit from a brief explanation of what constitutes a 'species-irrelevant' input (e.g. primate-designed enrichment used for reptiles).
- "Figure 1" must be enclosed in parentheses. Otherwise, a description of the figure must be included in this paragraph.
68-73. This is a very long title. This description should be included in the paragraph where Figure 1 is mentioned.
124-126. “Traditionally, zoos have relied on physical indicators (e.g., changes in body mass or body condition and health status)...”. The parenthetical list is a bit dense. Consider breaking it down: "such as body mass, body condition and general health".
126-129. Indicate why these output-based indicators are preferable or how their validity is tested (a brief mention of standards or frameworks would add rigour).
131-137. Here, reference is made to the "Five Domains Model", which explicitly includes affective states in the assessment of well-being. Consider including that reference (Mellor et al. 2020).
138-140. “Most predominant” is redundant. Use either “most used” or “predominant”.
142-149. Add a sentence recognising best practice to mitigate these problems (e.g. interobserver reliability testing, standardised ethograms).
150-152. Could briefly mention examples of remote systems being used successfully (e.g. machine vision systems).
153-157. Refer to the debate about “coping mechanisms” and the potential mismatch between observed behaviour and affective state.
221-224. Consider clarifying "knowing them" - does this refer to individual behavioural repertoires or species-level characteristics? Precision here would strengthen the argument.
225-226. Cite literature on agency and control.
226-227. Specify the species or taxa in which these effects have been observed. Generalisation may seem excessive without empirical support.
227-230. Suggested reference: Clark, 2017. “Cognitive enrichment and welfare: current approaches and future directions.”.
230-231. Consider rephrasing for flow: “However, understanding the intended outcomes of enrichment is essential before its design...”.
231-236. Introduce the notion of “goal-oriented enrichment” as a formal term if used later.
236-238. Ensure Figure 2 is legible and clearly linked to the text. Add brief explanation of what each step demonstrates.
240-245. Same as Figure 1. (lines 68-73). The caption is overly long and partly redundant. Focus on the function of the figure: “Species-specific, evidence-based enrichment plans begin by defining the behavioural goal, followed by implementation, monitoring, and welfare-linked evaluation.”.
246-251. Mention the necessity of replication across contexts (environments, populations, seasons).
251-255. Briefly explain what this document includes.
336-339. “A focus on creating positive environments may be more effective than assessing emotional states...” (table). This is an important point, especially for taxa with limited observable affect. Suggest rephrasing: “While emotional state assessment remains challenging in many taxa, prioritizing environments that facilitate positive outcomes may offer more practical welfare inferences.”.
336-339. “A sound knowledge of habitat and natural history...”. Include an example where this alignment led to measurable welfare improvements.
340-343. Sentence structure is fragmented. Suggest: “Although zoo welfare research often focuses on a limited range of species [16,43], these models can offer transferable methods and inform broader care strategies.”.
350-352. Specify what “collaborative efforts” might look like: cross-institutional studies, shared databases?
353-356. Clarify what these limitations are: subjectivity? lack of quantification? Add one sentence to unpack the critique.
Author Response
Reviewer 4
General concept comments
Article
This manuscript addresses a crucial issue in zoo animal welfare: the balance between input- and output-based indicators, and the need for evidence-based systems that take into account the complexity of welfare assessment. However, certain stylistic and structural refinements are required to bring it to publication-ready status.
Review
Specific comments
14-17. "This paper examines the current state of welfare priorities in Zoos...". The repetition of the words 'welfare' and 'zoos' reduces the stylistic elegance. Reword: “This paper re-evaluates current welfare frameworks in zoological institutions, advocating for…”.
Thank you for the feedback, we have edited this accordingly.
17-20. To improve clarity and reinforce the problem being addressed, suggest adding 1-2 examples of these limitations here.
Thank you for the feedback. We have edited with examples of limitations according to this suggestion.
20-23. This could benefit from a brief explanation of what constitutes a 'species-irrelevant' input (e.g. primate-designed enrichment used for reptiles).
Thank you for the feedback. We hope that we have addressed this in our response and edit based on the review of line 17-20. We are mindful of the word limit of the abstract.
Line 62 "Figure 1" must be enclosed in parentheses. Otherwise, a description of the figure must be included in this paragraph.
Edited accordingly.
68-73. This is a very long title. This description should be included in the paragraph where Figure 1 is mentioned.
Thank you for the feedback. We have integrated the original caption into the main body of the text and we have reduced the length of the caption itself.
124-126. “Traditionally, zoos have relied on physical indicators (e.g., changes in body mass or body condition and health status)...”. The parenthetical list is a bit dense. Consider breaking it down: "such as body mass, body condition and general health".
Thank you for the feedback. We have edited this information based on the suggestions of the reviewer. We hope this clarifies the information presented here.
126-129. Indicate why these output-based indicators are preferable or how their validity is tested (a brief mention of standards or frameworks would add rigour).
Thank you for the feedback. We have expanded this section with an example of how such testing could work and why this would be beneficial to validating inferences of welfare outputs.
131-137. Here, reference is made to the "Five Domains Model", which explicitly includes affective states in the assessment of well-being. Consider including that reference (Mellor et al. 2020).
Thank you for the feedback. We have amended this accordingly.
138-140. “Most predominant” is redundant. Use either “most used” or “predominant”.
Thank you for the feedback. We have edited accordingly.
142-149. Add a sentence recognising best practice to mitigate these problems (e.g. interobserver reliability testing, standardised ethograms).
This section has been changed based on other reviewer feedback to include the points noted here. We hope the edit covers your suggested alteration.
150-152. Could briefly mention examples of remote systems being used successfully (e.g. machine vision systems).
Thank you for the feedback. We have edited this accordingly and provided examples.
153-157. Refer to the debate about “coping mechanisms” and the potential mismatch between observed behaviour and affective state.
Thank you for the feedback. We have extended this section to discuss the concept of coping and the challenge of understanding affective state from behaviour. We have included new references to support these points.
221-224. Consider clarifying "knowing them" - does this refer to individual behavioural repertoires or species-level characteristics? Precision here would strengthen the argument.
Thank you for the feedback. We have changed “knowing” to understanding and added in evolutionary context.
225-226. Cite literature on agency and control.
Thank you for the feedback. We have included citations here.
226-227. Specify the species or taxa in which these effects have been observed. Generalisation may seem excessive without empirical support.
Thank you for the suggestion. We have edited to include specific examples.
227-230. Suggested reference: Clark, 2017. “Cognitive enrichment and welfare: current approaches and future directions.”.
Thank you for the feedback. We have provided two additional citations to our argument here.
230-231. Consider rephrasing for flow: “However, understanding the intended outcomes of enrichment is essential before its design...”.
Thank you for the useful suggestion. We have amended this sentence accordingly.
231-236. Introduce the notion of “goal-oriented enrichment” as a formal term if used later.
Thank you for the feedback. We have re-phrased this section to include a description of this term.
236-238. Ensure Figure 2 is legible and clearly linked to the text. Add brief explanation of what each step demonstrates.
Thank you for the feedback. We will submit the image as a file of the full sized image with out revisions to ensure the best quality image can be provided. We have also extended our interpretation of this figure in the text.
240-245. Same as Figure 1. (lines 68-73). The caption is overly long and partly redundant. Focus on the function of the figure: “Species-specific, evidence-based enrichment plans begin by defining the behavioural goal, followed by implementation, monitoring, and welfare-linked evaluation.”.
Thank you for the feedback. We have amended the figure accordingly.
246-251. Mention the necessity of replication across contexts (environments, populations, seasons).
Thank you for the suggested inclusion. We have added a statemen into the text.
251-255. Briefly explain what this document includes.
Thank you for the feedback. We have provided a description of this document.
336-339. “A focus on creating positive environments may be more effective than assessing emotional states...” (table). This is an important point, especially for taxa with limited observable affect. Suggest rephrasing: “While emotional state assessment remains challenging in many taxa, prioritizing environments that facilitate positive outcomes may offer more practical welfare inferences.”.
Thank you for the suggestion. We have rephrased this aspect of the table according to this revision.
336-339. “A sound knowledge of habitat and natural history...”. Include an example where this alignment led to measurable welfare improvements.
We have provided two references to support this statement.
340-343. Sentence structure is fragmented. Suggest: “Although zoo welfare research often focuses on a limited range of species [16,43], these models can offer transferable methods and inform broader care strategies.”.
Thank you for the feedback. We had similar feedback from another reviewer and thus we have edited this section already. We hope that is answers your critique too.
350-352. Specify what “collaborative efforts” might look like: cross-institutional studies, shared databases?
We have included these suggestions in our paper. Thank you for the feedback.
353-356. Clarify what these limitations are: subjectivity? lack of quantification? Add one sentence to unpack the critique.
Thank you for the feedback. We have provided a critique of these limitations accordingly.
Round 2
Reviewer 2 Report
Comments and Suggestions for AuthorsThe contribution offers valuable insights for improving animal welfare management and assessment practices, emphasizing the importance of an integrated and scientifically grounded approach.The article has shown considerable improvement compared to the previous version; however, there are several areas that could benefit from further clarification or elaboration to strengthen the scientific rigor and coherence of the arguments. I
In attached, you will find a detailed list of comments suggesting possible improvements. I hope these will be helpful in refining your work and enhancing its overall impact.
Comments for author File: Comments.pdf
Author Response
General comments
The article has shown considerable improvement compared to the previous version; however, in my
view, it is still not fully ready for publication. The connection to animal welfare remains unclear, as
certain aspects remain quite general and would benefit from further elaboration. Additionally, I believe that two key concerns persist.
Thank you for the comment. We are unsure as to the phrase “the connection to animal welfare remains unclear” when the entire paper is focussed on evidence for appropriate inputs that support species-specific positive welfare outputs in zoos and aquariums.” We have reviewed a wide range of articles to show the importance of correct inputs (that are based on data and thus likely to be most relevance for specific species) to how zoo and aquarium animals can experience positive welfare outputs. If the reviewer can provide explanation for how our paper does not link to welfare, then we can certainly try to amend this but we do not understand how this paper lacks clarity in its current form. We have amended the introduction to make sure that we are clear on how we link the need for evidence with how we consider meaningful assessment of welfare. We have thus edited the aims of our paper.
- The authors set highly ambitious and commendable objectives regarding the role of their
manuscript in enhancing the understanding and promotion of animal welfare. For instance, they
state: "By evaluating the limitations of 17 current welfare practices (e.g., a lack of species specific
assessment protocols or sound husbandry evidence to base measures on) and presenting
potential areas for improvement, this research aims to establish a sound baseline for meaningful
welfare outputs, focusing on both physical and psychological well-being of zoo animals."
However, the article does not yet fully meet these objectives, as it remains somewhat broad and
does not establish a sufficiently strong foundation for understanding, measuring, or promoting
animal welfare.
Thank you for the feedback. We have edited this statement for clarity and to ensure that we do not overreach ourselves. Our paper aims to show why relevant, evidence-based inputs are required as the support for good welfare outputs. Our paper reviews the need for evidence to show what is currently lacking for zoo welfare outputs to be positive or indeed measured in a meaningful way. We have clearly focused on why it is important to ensure we collect evidence for welfare-focussed inputs to support attainment of species-specific outputs. We have also added a sentence to make clear that we are not advocating for using inputs / factors only, but rather for using a combination of outputs and inputs / factors (lines 69-71).
- The discussion surrounding inputs could be further clarified, particularly in terms of their
measurement and their specific contributions to welfare. More concrete examples would be
beneficial in illustrating both the process of assessment and the resulting impact on animal wellbeing. Specifically, when measuring an input, what insights does it provide regarding the welfare
status of the animals?
We have clarified what is meant by inputs and these have been reworded as “factors” based on other reviewer feedback. We have included further citations to support the points that we have made, and to ensure we have a comprehensive review of the literature. Edits and inclusion of new examples are included in yellow highlight.
There are already numerous guidelines on zoo animal management, habitat design, diet composition, and appropriate enrichment practices, all aiming to minimize negative effects and maximize positive outcomes for welfare. While the authors may wish to emphasize the need for further studies in this area, the article does not yet present a clearly defined methodology for standardizing input measurements, nor does it offer specific examples to illustrate this approach.
There are indeed guidelines available, but they do not cover all taxa and nor are they always peer reviewed. The literature states that many species are not the focus of evidence gathering research and thus this means extrapolation from other taxa, which may be incorrect. We are explaining the need to continue to both collect and review evidence for species-specific inputs to make sure they are relevant to the animals we are keeping. Without these appropriate inputs, animals will not experience positive emotional outputs because their environment will not be suitable.
Highlights
- Completeness of Citations When claims are made regarding the relative effectiveness of different
approaches, it would be helpful to include references to relevant studies to support the arguments
presented.
Thank you for the comment. We are unsure what this means, “the completeness of citations”? We have provided a citation to support examples and arguments included when these have been taken from wider reading, and we have extended the number of references used. We have also included further citations based on the feedback of previous reviewers.
- Balance Between Input and Output Measures The comparison between the use of input and output
measures appears to focus exclusively on the assessment of animals' emotional states. It would be
beneficial to broaden the discussion to include other output indicators, which may be simpler and more effective for evaluating animal welfare.
Thank you for the comment. We have explained that other outputs also need consideration, for example behaviour, but if we are going to advocate for mental outputs (as per the Five Domains) then we need to understand that input based factors have to be correct if the animal is to experience positive moods. Indeed, in lines 132-135 we provide a list of some of the main output-based indicators, that include not only emotional states, but also clinical signs, prevalence of disease, body condition and behaviour, among others.
Many of the statements regarding the effectiveness of input measures are based on general concepts. Where possible, it would be helpful to include empirical data, comparative studies, or concrete case examples demonstrating how specific inputs have led to tangible improvements in zoological settings.
Thank you for the comment. There are indeed many examples of how specific inputs have led to tangible improvements in zoological settings and a review of those would fall well beyond the scope of our paper. However, we have added a paragraph explaining how the effects of specific inputs on animal welfare can be assessed (lines 501-508)
Expanding on the Limitations of the Input-Based Approach
It would be valuable to also consider the practical challenges associated with an input-based model. For example:
What are the difficulties in identifying optimal inputs for each species?
How do environmental context and individual variability influence the effectiveness of input
measures?
Addressing these questions would contribute to a more balanced and comprehensive discussion of the approach. The article could benefit from a more structured section on methodologies for evaluating input measures, potentially including suggestions for specific protocols or tools to assess their impact.
Thank you for the comment. We have included a paragraph that summarizes the main practical challenges associated with an input-based model (lines 555-560). And we have reviewed the entire paper to check balance in our arguments.
- Coherence and Logic The statement suggesting that, rather than measuring emotional states, we
should focus on creating favourable conditions to promote positive emotional experiences in animals
lacks concrete verification. How can we be certain that the conditions created truly result in emotional well-being? It is important to highlight the role of output indicators in validating such an assumption.
We are unsure of the reviewer’s comments here as we do not just focus on emotional states but rather we have reviewed and explained how evidence based approaches (to care) provide the best foundation for animals to experience positive emotional outputs. An animal in an incorrect environment that does not provide access to resources in a beneficial or biologically relevant way is not going to experience long-term positive welfare outcomes.
- Strengthening the Conclusions The manuscript would benefit from a final section that clearly
summarizes how the research findings can be applied to the management of animal welfare in zoos and aquariums. Highlighting the practical implications of the study would help reinforce its relevance and impact.
Thank you for the feedback. We have provided a new end to the existing conclusions to summarise the main theme of the manuscript, including the need for more scientific evidence on how inputs can lead to positive outputs.
- Some phrases need to be reviewed and further elaborated, in my opinion.
Example:
(line 100-106)
I respectfully disagree with this statement. It overlooks the fact that animals reintroduced from
zoos though only a small fraction compared to the population that remains in captivity undergo
pre-release training to prepare them for life in the wild. This process reinforces key survival traits,
such as fear of humans, which are essential for their well-being in natural environments.
However, fostering these same traits within zoos can have negative effects on animal welfare. For
instance, an animal that develops a fear of keepers and visitors is more likely to experience
heightened stress levels. Therefore, I believe the concluding statement that inputs should aim to maintain animals as wild in
order to promote their welfare is somewhat misleading and should be reconsidered.
Thank you for the feedback. We have edited the final sentence to state that adaptive traits need to be maintained in zoo animals in ex situ populations. Without the conservation of such adaptive traits, zoo animals cannot be meaningfully involved in One Plan Approaches to conservation, for example. We have attempted to integrate this into the text.
(line 199-206)
There is a lack of references supporting the claim that an input-based approach is more promising
and effective than an output-based approach it would be beneficial to include citations from
relevant literature to substantiate this perspective. Additionally, the comparison between input use and output indicators focuses solely on the assessment of emotional state as an output indicator. However, there are multiple other output based indicators that provide more reliable and practical assessments of animal welfare beyond emotional state evaluations. preferable to create conditions that foster a positive emotional state, raises an essential question: how can we confirm that the implemented conditions truly result in a positive emotional state? To verify this, it is necessary to utilize output indicators. Thus, the focus on input-based approaches appears somewhat inconsistent. If the effectiveness of these inputs cannot be validated without output measures, what is the rationale for prioritizing them?
Thank you for the comment. We do not just focus on emotional outputs and, as already mentioned, we provide a list of the main output indicators, including those related with nutrition (for example, body condition), health (including clinical signs and the prevalence of diseases) and behaviour. Please notice that we are not at all advocating for using inputs only, but for using a combination of both inputs and outputs. We have added a sentence to clarify this (see previous comments).Indeed, the main idea of our paper is that we should not focus on output-based indicators, more that we need to ensure that care is correct. We hope to have clarified this in our conclusion.
Reviewer 3 Report
Comments and Suggestions for AuthorsUpon revision, the authors have markedly improved the manuscript. The flow is much clearer and it is easier to understand and interpret the meaning behind the manuscript. It is therefore evident that the authors have made an effort to address the comments raised on the previous version of the manuscript. There are a few points that require attention however, most important of which is the terminology used in describing input-based measures/resource-based indicators. This particular element must be addressed as it is fundamental to the interpretation of the rest of the manuscript and reflects a conflation of ideas. Otherwise, the manuscript should be proof-read prior to resubmission. Below is the specific feedback relating to the first revision of the manuscript.
Page 4
Lines 120-152 The terminology here does not seem appropriate. The authors define two types of measures, namely output-based measures (animal-based indicators) and input-based measures (resource-based indicators). I agree entirely with the contextualisation and presentation of the former. However, the latter again strikes me as an issue. The problem lies in the assignment of these features to the role of measures/indicators. How does one measure 'appropriateness', 'design' or 'relevance'? If the terms 'measure' or 'indicator' are to be used, then the implication is that the factor under consideration can be quantified in welfare terms or involves a consistent relationship to welfare; in the context presented, this is not possible. The appropriateness of factors such as enclosure size, environmental enrichment and thermal conditions cannot be quantified independently of the animal under consideration and therefore cannot be termed 'measures'. Similarly, these are not linked to welfare state in a consistent, reliable and predictable way (e.g. a small enclosure may have no negative consequences when housing a hedgehog but may be detrimental to a horse) and may even vary from individual to individual (e.g. some individual animals benefit from auditory enrichment whereas others find it aversive) and thus cannot be termed 'indicators'. As pointed out in the previous round of review and affirmed by the authors themselves here (lines 136-138), these are not indicators/measures of welfare because they only become relevant to welfare once they are reliably coupled with an output-based measure. Using the example provided by the authors, whether a species has been housed in an appropriately sized and designed exhibit can only be determined by comparison of the animal-based indicators of an individual once in that exhibit. How each individual animal perceives the space that they live in and is able to operate therein will determine whether the space is 'appropriately sized and designed'. The size and design is not, in and of itself, 'appropriate' without understanding how some measure of welfare is affected by it (as stated in the previous feedback, what is appropriate for one species is not appropriate for all species, and so appropriateness itself is a relativistic concept). One cannot determine the welfare impact based solely on how large their enclosure is, nor could one reliably determine the relevance of enrichment or climate conditions without measuring how welfare indicators (output-based measures) respond. Thus, labelling the physical characteristics of the space as an 'indicator'/'measure' of welfare is logically unfounded. That is not to say that they do not play a role; on the contrary, factors such as the size and design of the physical housing of an animal, the environmental enrichment provided and the environmental conditions the animal is subjected to are critical in determining welfare state and in many way form the foundation to generating good welfare. To this end, the authors are correct in identifying the relevance of these in relation to welfare state and assessment. However, they are not indicators/measures of welfare - they are factors/drivers which affect welfare. I suggest that the terms 'contributing factors' or 'drivers' be used in place of 'measures' and 'indicators' in the context of input/resource-centred factors in welfare. The terminology used must be corrected because it conflates mechanism and measurement.
Page 5
Lines 181-186 This is also true of behaviours which are not inherently abnormal but may be expressed in ways which are not species/context-appropriate (e.g. space use: Duncan, L.M., D’Egidio Kotze, C., Pillay, N. Long-term spatial restriction generates deferred limited space use in a zoo-housed chimpanzee group. Animals 2022, 12. https://doi.org/10.3390/ani12172207; displacement/vacuum behaviour: Kennedy, J.S. Displacement activities and post-inhibitory rebound. Anim. Behav. 1985, 33, 1375–1377, doi:https://doi.org/10.1016/S0003-3472(85)80207-4, Mason, G. Stereotypic behaviour in captive animals: fundamentals and implications for welfare and beyond. 2006, 325-356 IN: Stereotypic animal behaviour: fundamentals and applications to welfare. EDs: Mason, G, Rushen, J. 2nd Ed. CABI Press. https://doi.org/10.1079/9780851990040.0325)
Page 6
Line 225 Do the authors mean 'ectothermic' (it is written as ‘ecothermic’)? Check the spelling here. Also, some endothermic species may also fall within this assessment category (e.g. many bird species). Perhaps it would be helpful to rather categorise this group as 'non-mammalian' species.
Figure 3
The figure presented illustrates basic good scientific practice in ensuring validity, accuracy and precision. It is not clear why this has been included. It does not add anything novel or illustrate a concept that could not be presented in a single sentence in the text. This should be removed.
Author Response
Reviewer 3 responses
Upon revision, the authors have markedly improved the manuscript. The flow is much clearer and it is easier to understand and interpret the meaning behind the manuscript. It is therefore evident that the authors have made an effort to address the comments raised on the previous version of the manuscript. There are a few points that require attention however, most important of which is the terminology used in describing input-based measures/resource-based indicators. This particular element must be addressed as it is fundamental to the interpretation of the rest of the manuscript and reflects a conflation of ideas. Otherwise, the manuscript should be proof-read prior to resubmission. Below is the specific feedback relating to the first revision of the manuscript.
Thank you for the positive feedback. We have reviewed the manuscript for spelling and grammar, and we have actioned all edits below. We appreciate the thorough and useful review to improve the paper.
Page 4
Lines 120-152 The terminology here does not seem appropriate. The authors define two types of measures, namely output-based measures (animal-based indicators) and input-based measures (resource-based indicators). I agree entirely with the contextualisation and presentation of the former. However, the latter again strikes me as an issue. The problem lies in the assignment of these features to the role of measures/indicators. How does one measure 'appropriateness', 'design' or 'relevance'? If the terms 'measure' or 'indicator' are to be used, then the implication is that the factor under consideration can be quantified in welfare terms or involves a consistent relationship to welfare; in the context presented, this is not possible. The appropriateness of factors such as enclosure size, environmental enrichment and thermal conditions cannot be quantified independently of the animal under consideration and therefore cannot be termed 'measures'. Similarly, these are not linked to welfare state in a consistent, reliable and predictable way (e.g. a small enclosure may have no negative consequences when housing a hedgehog but may be detrimental to a horse) and may even vary from individual to individual (e.g. some individual animals benefit from auditory enrichment whereas others find it aversive) and thus cannot be termed 'indicators'. As pointed out in the previous round of review and affirmed by the authors themselves here (lines 136-138), these are not indicators/measures of welfare because they only become relevant to welfare once they are reliably coupled with an output-based measure. Using the example provided by the authors, whether a species has been housed in an appropriately sized and designed exhibit can only be determined by comparison of the animal-based indicators of an individual once in that exhibit. How each individual animal perceives the space that they live in and is able to operate therein will determine whether the space is 'appropriately sized and designed'. The size and design is not, in and of itself, 'appropriate' without understanding how some measure of welfare is affected by it (as stated in the previous feedback, what is appropriate for one species is not appropriate for all species, and so appropriateness itself is a relativistic concept). One cannot determine the welfare impact based solely on how large their enclosure is, nor could one reliably determine the relevance of enrichment or climate conditions without measuring how welfare indicators (output-based measures) respond. Thus, labelling the physical characteristics of the space as an 'indicator'/'measure' of welfare is logically unfounded. That is not to say that they do not play a role; on the contrary, factors such as the size and design of the physical housing of an animal, the environmental enrichment provided and the environmental conditions the animal is subjected to are critical in determining welfare state and in many way form the foundation to generating good welfare. To this end, the authors are correct in identifying the relevance of these in relation to welfare state and assessment. However, they are not indicators/measures of welfare - they are factors/drivers which affect welfare. I suggest that the terms 'contributing factors' or 'drivers' be used in place of 'measures' and 'indicators' in the context of input/resource-centred factors in welfare. The terminology used must be corrected because it conflates mechanism and measurement.
Thank you for the feedback. We have edited this section to include the word factor in place of measure or indicator when referring to input-based approaches. We hope this makes this section of the paper clearer.
Page 5
Lines 181-186 This is also true of behaviours which are not inherently abnormal but may be expressed in ways which are not species/context-appropriate (e.g. space use: Duncan, L.M., D’Egidio Kotze, C., Pillay, N. Long-term spatial restriction generates deferred limited space use in a zoo-housed chimpanzee group. Animals 2022, 12. https://doi.org/10.3390/ani12172207; displacement/vacuum behaviour: Kennedy, J.S. Displacement activities and post-inhibitory rebound. Anim. Behav. 1985, 33, 1375–1377, doi:https://doi.org/10.1016/S0003-3472(85)80207-4, Mason, G. Stereotypic behaviour in captive animals: fundamentals and implications for welfare and beyond. 2006, 325-356 IN: Stereotypic animal behaviour: fundamentals and applications to welfare. EDs: Mason, G, Rushen, J. 2nd Ed. CABI Press. https://doi.org/10.1079/9780851990040.0325)
Thank you for the examples and suggested references. We have included these in the text and added in the explanation of behaviours being performed out of context, and what this means for welfare assessment.
Page 6
Line 225 Do the authors mean 'ectothermic' (it is written as ‘ecothermic’)? Check the spelling here. Also, some endothermic species may also fall within this assessment category (e.g. many bird species). Perhaps it would be helpful to rather categorise this group as 'non-mammalian' species.
We have edited this accordingly. Thank you for the suggestion.
Figure 3
The figure presented illustrates basic good scientific practice in ensuring validity, accuracy and precision. It is not clear why this has been included. It does not add anything novel or illustrate a concept that could not be presented in a single sentence in the text. This should be removed.
Thank you for the feedback. We have removed the figure from the main manuscript and we have renumbered all other figures accordingly.
Round 3
Reviewer 2 Report
Comments and Suggestions for AuthorsThanks to the revisions made, expecially the last ones— the addition of new statements, references, and, most importantly, the elaboration on specific sections and the clarification of certain points —the article is now satisfactory. As a result, the parts I previously found too general have now been clarified, significantly improving the overall quality of the article.
Author Response
Thanks to the revisions made, expecially the last ones— the addition of new statements, references, and, most importantly, the elaboration on specific sections and the clarification of certain points —the article is now satisfactory. As a result, the parts I previously found too general have now been clarified, significantly improving the overall quality of the article.
Thank you for the positive feedback on our manuscript. We are pleased that the revisions have made the paper stronger and have provided a clearer narrative. We thank the reviewer for their supportive and helpful comments, edits and ideas for revision.