Identifying Essential Elements of Good Giraffe Welfare—Can We Use Knowledge of a Species’ Fundamental Needs to Develop Welfare-Focussed Husbandry?
Round 1
Reviewer 1 Report (Previous Reviewer 2)
First, I would like to thank and congratulate the author for the effort provided to enhance the scientific quality outcome of this paper.
Indeed, the revised version of the manuscript sounds well constructive. The added citations and precisions have largely improved the content of this paper.
The author specific professional qualities are well implemented throughout the present work.
I have no more remarks and comments. I approve the present version.
Author Response
First, I would like to thank and congratulate the author for the effort provided to enhance the scientific quality outcome of this paper.
Indeed, the revised version of the manuscript sounds well constructive. The added citations and precisions have largely improved the content of this paper.
The author specific professional qualities are well implemented throughout the present work.
I have no more remarks and comments. I approve the present version.
Thank you for the useful and helpful review of the paper and the approval of the finished manuscript.
Reviewer 2 Report (Previous Reviewer 3)
The author has done a significant effort to improve the manuscript and succeed in it. Well done! I hope the author thinks that my review helped him to present a better version of the manuscript.
I think that now it is suitable for publication. I add just a very few (and very small) comments:
Line 160: The scientific name has already been mentioned (line 81), so it is not necessary here.
Figure 2: there is a “triangular” in the definition of picture 3 that should be removed.
Line 237: Enrichment IS always useful?
Lines 329-336: The right side of this paragraph must be justified.
Line 356: It is just a suggestion but: “the paper hopes to encourage… by encouraging…” Perhaps replacing one of the two “encourage” with a synonym could be better?
Lines 356-360: Is there any specific reason to select these species besides the idea of “using the concept behind W-E-L-F-A-R-E in a diverse and abroad variety of species? Maybe adding something to clarify this?
Author Response
Thank you for the helpful and relevant feedback on this paper. It is much appreciated. All comments have been actioned below.
The author has done a significant effort to improve the manuscript and succeed in it. Well done! I hope the author thinks that my review helped him to present a better version of the manuscript.
Very useful comments and suggestions. Thank you.
I think that now it is suitable for publication. I add just a very few (and very small) comments:
Line 160: The scientific name has already been mentioned (line 81), so it is not necessary here.
Edited
Figure 2: there is a “triangular” in the definition of picture 3 that should be removed.
Edited
Line 237: Enrichment IS always useful?
Edited
Lines 329-336: The right side of this paragraph must be justified.
Edited
Line 356: It is just a suggestion but: “the paper hopes to encourage… by encouraging…” Perhaps replacing one of the two “encourage” with a synonym could be better?
Edited the second encouraging.
Lines 356-360: Is there any specific reason to select these species besides the idea of “using the concept behind W-E-L-F-A-R-E in a diverse and abroad variety of species? Maybe adding something to clarify this?
I have removed the selected species and just stated across all taxonomic groups.
This manuscript is a resubmission of an earlier submission. The following is a list of the peer review reports and author responses from that submission.
Round 1
Reviewer 1 Report
The author presents an interesting review on the welfare of giraffe. Study design and research questions are clearly described. In this sense, it is easy to understand the aim of this study. The bright side of the manuscript is that to provide some useful practical details on related topic. In this context, the study contributes to animal welfare. I can only say a few words to improve the manuscript.
In my opinion, as a zoo-housed species the giraffe is a well-known species, but the natural disturbance and conservation status of the giraffe can be given before the line 126 with 2-3 sentences. Moreover, importance of zoos and captive care for the future of species can be mentioned in the discussion section with several sentences. In this way, importance of WELFARE can be highlighted.
Author Response
Replies to reviewer 1
The author presents an interesting review on the welfare of giraffe. Study design and research questions are clearly described. In this sense, it is easy to understand the aim of this study. The bright side of the manuscript is that to provide some useful practical details on related topic. In this context, the study contributes to animal welfare. I can only say a few words to improve the manuscript.
In my opinion, as a zoo-housed species the giraffe is a well-known species, but the natural disturbance and conservation status of the giraffe can be given before the line 126 with 2-3 sentences. Moreover, importance of zoos and captive care for the future of species can be mentioned in the discussion section with several sentences. In this way, importance of WELFARE can be highlighted.
Thank you for the comments. I have edited the discussion accordingly to further explain the importance of zoos to the future survival and conservation. I am about unsure as to your first suggestion, as the key concepts of good husbandry to promote welfare are grounded in the introduction, with the giraffe being the applied example. Hence why I devote section 3 onwards specifically to the giraffe after the relevance of easy-to-understand welfare indictors has been introduced.
Reviewer 2 Report
The present work “Spelling out zoo animal welfare needs: An applied example using a familiar but specialised species” constitutes an ambitious contribution in assessing captive zoo-animal welfare. The author, field specialist, suggested some practical keys to optimize what is called “welfare-focussed husbandry”. To spell out these welfare needs, the author has chosen the giraffe, a familiar zoo-housed species, as an example and formulate a seven step guide including fundamental and specific concepts.
The manuscript is well written and structured; but, differs from ordinary papers.
The abstract is lucid and concise. It includes all the aspects raised in this document and describes and justifies the suggested stepwise approach. However, I suggest withdrawing “bridging the gap” from the “keywords”.
The introduction is conforming. It introduces, defines and justifies the topic of the present work by including some relevant references.
Thereafter, the author presents a literature synthesis of animal wants and needs and specifically spells out welfare needs of the concerned zoo-housed species: the giraffe. Meanwhile, the author has omitted to evoke some specific situations, for example the coupling, mating and gestation period as well as the new born care.
Concerning the suggested seven step welfare guide, they were defined and described; but, apparently, the author deliberately aims to get seven steps to fulfil the seven letters of WELFARE (W: warmth, E: enrichment, L: leaves, F: feeding, A: alfalfa, R: rumination and E: exercise); while, the third, the fourth and fifth steps are all involved in feeding process. Meanwhile, other specific steps should be added particularly Rest, new-born care and coupling-mating.
Globally, I praise the effort provided by the author to establish such animal welfare monitoring process; which, still, should be validated by zoo-professional animal care.
Author Response
Replies to reviewer 2
The present work “Spelling out zoo animal welfare needs: An applied example using a familiar but specialised species” constitutes an ambitious contribution in assessing captive zoo-animal welfare. The author, field specialist, suggested some practical keys to optimize what is called “welfare-focussed husbandry”. To spell out these welfare needs, the author has chosen the giraffe, a familiar zoo-housed species, as an example and formulate a seven step guide including fundamental and specific concepts.
The manuscript is well written and structured; but, differs from ordinary papers.
The abstract is lucid and concise. It includes all the aspects raised in this document and describes and justifies the suggested stepwise approach. However, I suggest withdrawing “bridging the gap” from the “keywords”.
Thank you for the suggestion. The keywords have been edited.
The introduction is conforming. It introduces, defines and justifies the topic of the present work by including some relevant references.
Thereafter, the author presents a literature synthesis of animal wants and needs and specifically spells out welfare needs of the concerned zoo-housed species: the giraffe. Meanwhile, the author has omitted to evoke some specific situations, for example the coupling, mating and gestation period as well as the new born care.
Thank you for the feedback. I have provided a comment in discussion that WELFARE could be extended to WELFARE + for research and refinement of correct care for breeding animals and young. However, the clear focus of this paper is on what are the essential needs of a zoo housed giraffe to maintain excellent behavioural, physical and psychological health and I feel this aim is the most important.
Concerning the suggested seven step welfare guide, they were defined and described; but, apparently, the author deliberately aims to get seven steps to fulfil the seven letters of WELFARE (W: warmth, E: enrichment, L: leaves, F: feeding, A: alfalfa, R: rumination and E: exercise); while, the third, the fourth and fifth steps are all involved in feeding process. Meanwhile, other specific steps should be added particularly Rest, new-born care and coupling-mating.
Thank you for the feedback, I have clarified that new born care / reproduction can be refined and reviewed in an extension of this model for good welfare. Rest is part of rumination, and I have clarified this. But rumination is the crucial need for giraffes to be content and relaxed in the zoo. I have edited accordingly and provided new references on rumination and resting. it’s not so much that I have deliberately wanted giraffe welfare needs to fit into the word welfare, but rather, the evidence from the literature seems to suggest that, as away of easy identification of fundamental needs, they do fit into the word itself.
Globally, I praise the effort provided by the author to establish such animal welfare monitoring process; which, still, should be validated by zoo-professional animal care.
Thank you for the feedback; I feel it an important step for all welfare indicators to be validated by those who care for the animal in the zoo. I have edited part of the discussion to include the importance of validation and the development of a specific giraffe welfare assessment process as an extension of this work.
Reviewer 3 Report
Reviewer comments to manuscript jzbg-2379892 entitled “Spelling out zoo animal welfare needs: An applied example using a familiar but specialised species”
In the present manuscript, the author presents and justifies 7 key elements for the welfare of zoo-housed giraffes with the aim to provide a very practical approach. He also advocates for a “welfare-focussed husbandry” (which seems, to me, a more fancy synonym of “good animal care”) and for other practices or approaches to the care of zoo animals (such as to consider the emotional state of an animal as the core of the welfare, the importance of behaviour for welfare, or the need for using the knowledge of an species -natural history, ecology, anatomy, physiology, etc.- to identify welfare needs). Although this approach is completely right and good, it is the one taken in many zoological institutions from years ago and the manuscript does not provide specific novelty in relation to the use of all these elements to identify general and species-specific welfare needs and fulfil them nor to expand them. The manuscript is well written. In general, I think the paper is creative and aims to generate valid tool for giraffe care. However, I think there are some main concerns in relation to the manuscript that prevent it from being published.
Along all the text, I have the constant impression that the manuscript promises “more” than what it is. From the title (that induces the misunderstanding of what the paper provides is a way, a tool, a method, to identify zoo animal welfare needs) till the discussion and conclusions. I think that the paper is a good review of existing literature on captive giraffe welfare, with a very interesting aim to make it practical and connect the available scientific knowledge with husbandry and caring tips for zoo staff. I think this is enough and can deserve publication if major changes are done correctly, but many contradictions arise if the manuscript pretends to be more than this. The manuscript certainly does not provide or show a process or tool or method to identify zoo animal welfare needs, nor changes the way welfare in zoos should be promoted and protected. The giraffe is not an “example of species” to show a method for protecting zoo animal welfare. Instead, the paper is a giraffe-focused paper, useful for giraffes only. In order to be published, I think that the whole idea of the manuscript should be deeply readjusted: the title, the introduction and discussion, etc. For instance, the title should state clearly that the paper presents a selection of important elements for captive giraffe welfare appropriately reviewed and with suggested practical implications.
I think author should take the current version of the manuscript as the basis for a future paper, but going much further in both directions: A) expandung the connection (justification) of his recommendations based on the natural feeding, habitat and behaviour of giraffes, as well as based on their anatomy, physiology, etc. (I miss information about the "ideal" amount of time a giraffe should be performing feeding behaviours, or the ideal amount of leaves or browse, or the specific nutritional requirements of the species, etc.); and B) detailing the practical information provided. With specific numbers, recommendations, suggested indicators to use, etc. making this paper really useful for zoo staff.
I have some other comments, suggestions and questions. I hope they could help the author to improve his research and to generate valid, reliable, new and useful knowledge.
ABSTRACT and INTRODUCTION
The info in the abstract and the introduction (and description of the aim of the paper) are slightly different (in the abstract the specificities of giraffes are mentioned -the WELFARE, etc., and seems to be more important, while in the introduction it seems that the giraffe is “just” an example. I think this is not the case. As mentioned previously, the tension between the introduction (the aims) and what the paper really is confuses me. In the aims seems that the paper provides a framework that is easily applied to several species, that is a “way to connect theory of welfare and knowledge of the biology of the species and daily caring routines”, with the giraffe as a simple example. However, later on the text is very focused on giraffes and it is not clear what were the processes to identify or create the “WELFARE list” for other species.
LINE 19: The idea of using the word WELFARE as a mnemonic tool to remember the presented elements or attributes to work on can be practical for zoo staff, but it can be a little bit confusing because the concept of “welfare” is already central for the proposed WELFARE, and then, the use of the word “welfare” is meaning two (already) connected things (the animal bell-being and the list of important attributes to check) that, however, are not the same. I suggest adding some differentiation in the text. Things such as using W-E-L-F-A-R-E or W.E.L.F.A.R.E, or g-WELFARE or similar.
SECTION 2.
LINES 97 -102: Serious doubts about it. And actually a dangerous statement. This sentence can led to the misunderstanding than providing the possibility to express consummatory phase is enough for fulfil all the behavioural needs (controversial but practical concept to use here) related to appetitive behaviour. Many examples (from exploring and foraging in tigers - 10.3390/ani10091536- to rooting in pigs -e.g. Broom and Jorhnson, 2019-) prove that this is not true, and that other behaviours related to feeding can be very important for the welfare, regardless of whether the animals are satiated at the end of the consummatory phase.
FIGURE 1: It seems interesting, but everything is too vague and general to be useful. How are these three points connected? What should readers “do” with the literature published about the anatomy and physiology of an species? What to look for? Is there any criteria to help navigating through all this literature? How do you consider and/or measure these aspects? What is exactly "measuring appetitive behaviour" for instance? Is this about time invested in? It is about frequency? You mention appetitive behaviour. But is this scheme useful for identifying other important behaviours?
LINES 120: “is not always achievable”. Seems to be "impossible". I suggest replacing it by "is not usually achieved" or "easily achievable" or adding a reference supporting the statement that is not achievable.
LINE 131: cause?
SECTION 3.
LINES 132-135: Where does this selection of issues come from? Do you have any reference of why these aspects are important, or any that support that the current management is solving these issues (care manuals or standards and guidelines, etc.)?
LINE 152: How is the giraffe WELFARE concept specifically helping training in giraffe behaviour? Maybe for giraffe care training...
LINES 155-157: it is not clear how this simplification and definitions of the core components and needs can be done. The author presents an example, already introduced by Hickey et al., so if giraffe is a species used as an example, it means that this can be applied (at some extent) to other species. How are the processes to actually define the core components and needs of a particular species? There is no information about them in the whole manuscript.
LINES 159-163: To me, this is the real outcome of the presented project. It is valuable enough and it probably deserves to be published, but the project does not go further than presenting a practical and scientifically-grounded checklist of critical elements for giraffe welfare protection and promotion.
FIGURE 2. I think that the pictures in this figure should be larger, considering that they provide visual information of examples about important aspects (not only beautiful or contextual). I also think that whether different pictures provide visual examples of different welfare indicators, they could be individually identified (each picture with a letter or number associated to the positive or negative specific indicator). I suggest the author to put the letters (WELFARE) in horizontal, with each letter (welfare-related element) associated to each picture (or pictures) placed above or below...
WARMTH SECTION: Despite some specific details are shown here (such as the fact that giraffes can die when exposed to <6ºC) and specific recommendations are shown in the table 1 (always >18ºC), I think that this paper (that claims the use of practical info about the giraffe as an example) is lacking some more detailed and practical information. The use of terminology such as "appropriate" is very dependant on each individual perception and should be replaced, when possible, with more rigorous and clear terms. Specifically, when talking about easy-to-measure elements, such as temperature. For example: what is "an adequate external temperature for outside access" in terms of ºC? Do we have scientific literature about temperature ranges of comfort in giraffes? What are the most evidence-based guidelines say about it?
ENRICHMENT SECTION: I miss some interesting and practical information, here. The importance of some type of enrichment seems to be clear. But what are the types of enrichment proved to work with giraffes? How tall they should be? What is "an appropriate social" group? In some species, one should expect almost an absolute absence of social conflicts, while in other one should expect certain conflicts without lesions or isolation, etc. What kind of feeders are better, why? I really miss more practical information. Without more detailed information, the giraffe WELFARE checklist is in a no man's land. It is no a deep literature review of the needs of giraffes nor a theoretical complete protocol for giraffe welfare assessment. But in the other hand, it is not detailed enough to be an updated guideline for giraffe care, with very practical information that could be easily followed by a zoo staff in the implementations of actions to improve giraffe welfare.
Encompassing under the same concept ("Enrichment") elements related to the collection plan and population management (social group), elements related to the daily management and care routines (using certain type of feeders, etc.), and elements related to facility design (the view across the paddock) seems to be a little bit "forced".
LINES 186-187: How do you suggest merging these two aspects? With a certain minimum facility surface? With design elements (barriers or other separations)?
LINE 189: I would say that enrichment is necessary and important always (some outside facilities can provide very low opportunities to express natural feeding behaviours without enrichment).
LEAVES: In comparison to Warmth and Enrichment, this section is much clearer and more practical (although the ideal amount of leaves/browse might be stated, even if very hard to achieve). What should be the ideal? is there any "minimum amount" to guarantee an adequate giraffes' endocrine and/or gastrointestinal health?
FEEDING:
LINE 219: Related to “at a several times per day”. Any recommendation? Several times could mean two or twenty depending on the reader. Is there any study recommending a minimum number of takes? Shall it be distributed along all day or during specific periods of time (day? night? etc.)? If this interesting manuscript tries to create something practical and based on natural history of giraffes, providing information regarding their activity budget and their daily biological rhythms could be very useful here.
Finding in "Rumination" information that would help the reader to understand how to be good in the "Feeding" section is not practical.
LINES 2019-220: Why are not specified in the present paper (referencing EAZA and other good guidelines)? According to the author, one of the manuscript’s aims is "iii) to move away from theoretical review of welfare definitions to encourage practitioners and animal care staff to look at their species". But this seems week when the recommendation is as simple as "Concentrate rations should be fed in weighed amounts for each individual animal in 215 the herd, at several times per day [...]". As mentioned before, I think author should take the current version of the manuscript as the basis for a future paper, but going much further in both directions: its connection with basic knowledge to identify giraffe needs and wants based on evolutionary ecology, anatomy and physiology, and behaviour, etc. and also making the manuscript much more detailed in requirements or recommendations (specific temperature degrees, expected amount of time ruminating, expected amount of leaves or browse, enrichment devices detailed, etc.).
Exercise: Aren't these, part of the enrichment goals?
LINE 250: are (instead of is)?
TABLE 1: In general, the table lists interesting aspects related to giraffe welfare, but the provision of information to facilitate an adequate answer is vague, affecting negatively one of the aims of the present manuscript, which is to create something practical. The Table 1 provides a list of potentially relevant welfare questions, but the provision of references that help zoo staff answering the suggested questions is not consistent.
In relation to warmth, there is the info related to >18ºC for indoor temperature (this is, to me, the example of what this giraffe WELFARE should look like. A place with justified specific references and recommendations that are important for welfare. Why there are no a minimum outside temperature? Is there any factor related to giraffes’ thermal comfort that changes between outside and inside (for instance, what can giraffes do to thermoregulate while outside?). Why does author not simply ask for ensuring that the giraffes are always >18ºC no matter where they are? Any explanation?
Related to enrichment: How does the author suggest assessing interest and engagement? it is a matter of using an ethogram and/or about investing a certain amount of time? What should be looked for? In relation to autonomy, If the author does not specify more, this question is tricky from a practical point of view. I can imagine many people being able to justify a YES and a NO for the same giraffe in relation to this point. The importance of choice and control for animal welfare is clear. And it is great that the author points it here. But "some" is a complex and subjective concept. One can say that the animal can go to the door of the facility and to the other extreme of the internal facility, or that the giraffe can sleep and move and smell, so this is "some" (enough) self-control over what they do. Others (like me) would consider that this is NOT ENOUGH degree of autonomy and that welfare issues may arise from this “not enough” degree of autonomy.
In relation to Leaves: Giraffes should be provided with browse ad libitum?
In relation to Feeding: That pelleted ration should be provided accordingly to animal weight and needs is obvious and widely accepted. What about placing in the paper the most updated list of nutritional requirements for the species? What about talking about the most common nutritional problems related to pellets (is there any particular element or nutrient in the pellets that tend to be wrongly prepared or calculated? Etc.). Ad “body” before “condition”. And regarding the Figure 2 reference, I think author should cite the specific picture in the figure.
In relation to Rumination: what is “a meaningful amount of time”? Any more objective way to assess it?. More importantly, the concept of “making the best possible efforts” is dangerous. As an informal recommendation, as a talk in a zoo, this might be fine. But as a scientific paper, I think good will is (sadly) not enough. Good will (making the best possible) does not guarantee good welfare in many zoos. I think focusing on "WHAT TO LOOK FOR, WHAT TO DO AND WHY" should be the basis of this paper, and WHAT TO DO or to ensure that all giraffes regularly ruminate each day and/or HOW TO ASSESS IT is what should be stated.
4. DISCUSSION
Part of the information here is essential to understand the previous section (section 3). I recommend an important restructuration of the manuscript because I think that the scientific justification for the 7 elements of the giraffe WELFARE (from the rationale to the specific suggested requirements) must be placed together.
LINES 263-267: Personally, I don't see the conflict between academic debate around theoretical concepts of welfare and the design and implement of best caring practices or guidelines (practice). To my knowledge, they actually benefit each other and, usually, they do not even compete for funding or resources. I would avoid using a non-existent debate between two critical elements of welfare to increase the perception of importance around the creation of practical welfare guidelines or literature.
LINES 280-281: The relationship between food quality and the affective state is not so direct. To my knowledge, welfare is not a binary concept but a continuous and gradual one. This means that poor-quality forage, and especially inappropriate forage, yes, they can have negative impact in the welfare of a giraffe, but experiencing a positive mental output is affected by many other factors (see the Five Domains Modell, for example: 10.3390/ani10101870).
TABLE 2: Especially the selection of the indicators, should be more specified and justified using references that connect the suggested indicators with the specific attribute aimed to evaluate.
Regarding warmth and enhanced longevity: Is this a valid indicator for warmth? the paper from Bercovitch and colleague does not test it. Problems with environmental temperature can reduce longevity, as problems with feeding, health care, stress... The connection between longevity and the attribute (Warmth) should be detailed.
Also, how is warmth related to the promotion of rumination? Please add a reference.
TABLE S1 (Line 300): In my opinion, Table S1 is important enough (and small enough) to be included in the main manuscript. Moreover, the table could be expanded with a description of the important elements seen in the videos or what to pay attention to (for instance, describing the characteristics that a feeder should have to increase foraging -feeding- time, what to look when assessing rumination and how to measure/record it, etc.).
LINE 301: “Once captive giraffes are provided with WELFARE”… the problem is that, in the present manuscript, there is no way to know whether a certain facility is providing WELFARE or not to the giraffes because it is not clear when and how to ensure that the 7-ítems list is enough followed or achieved. The lack of validated indicators correctly placed in each attribute, the lack of specific information to follow to understand whether enrichment, warmth, leaves, etc. are provided in ENOUGH quality and/or quantity, this makes the connection between WELFARE and the real welfare (the fifth domain) weak or vague. To me, one of the weaknesses of the manuscript is that it is a little contradictory that the manuscript is (to me, correctly) advocating for welfare-focused husbandry, for knowing the species in deep, for using evidence-based knowledge to improve giraffe care, etc. but at the same time, the manuscript is presenting a justified but vague checking list of elements or questions, without details on how or in which degree to achieve them, or how to assess them (even if they are focused on welfare indicators related to the four physical domains).
Lines 326-328: I think that, unfortunately, the current status of the manuscript does not allow the author to conclude this. There is not enough novel information, the rationale behind the WELFARE elements could be expanded and explored deeper (as well as their connection to giraffe biology and ecology), and the manuscript does not provide enough detailed information that can be followed to fulfil the needs related to the seven-step WELFARE elements or to assess if giraffe caring is successful or not.
LINE 361: But the paper does not provide clear information about how the use of this knowledge (on evolutionary ecology, anatomy and physiology, and behaviour of giraffes) helps the identification of giraffes' needs. Instead, it is the "classic" literature review, mostly based on (excellent) published papers on giraffe care, what has been done to support all the giraffe WELFARE proposal. To me, using this literature is good, but the paper does not create or show how to identify species-specific needs from the evolutionary ecology, anatomy, physiology, and behaviour of a particular species
Author Response
Replies to reviewer 3
In the present manuscript, the author presents and justifies 7 key elements for the welfare of zoo-housed giraffes with the aim to provide a very practical approach. He also advocates for a “welfare-focussed husbandry” (which seems, to me, a more fancy synonym of “good animal care”) and for other practices or approaches to the care of zoo animals (such as to consider the emotional state of an animal as the core of the welfare, the importance of behaviour for welfare, or the need for using the knowledge of an species -natural history, ecology, anatomy, physiology, etc.- to identify welfare needs). Although this approach is completely right and good, it is the one taken in many zoological institutions from years ago and the manuscript does not provide specific novelty in relation to the use of all these elements to identify general and species-specific welfare needs and fulfil them nor to expand them. The manuscript is well written. In general, I think the paper is creative and aims to generate valid tool for giraffe care. However, I think there are some main concerns in relation to the manuscript that prevent it from being published.
Along all the text, I have the constant impression that the manuscript promises “more” than what it is. From the title (that induces the misunderstanding of what the paper provides is a way, a tool, a method, to identify zoo animal welfare needs) till the discussion and conclusions. I think that the paper is a good review of existing literature on captive giraffe welfare, with a very interesting aim to make it practical and connect the available scientific knowledge with husbandry and caring tips for zoo staff. I think this is enough and can deserve publication if major changes are done correctly, but many contradictions arise if the manuscript pretends to be more than this. The manuscript certainly does not provide or show a process or tool or method to identify zoo animal welfare needs, nor changes the way welfare in zoos should be promoted and protected. The giraffe is not an “example of species” to show a method for protecting zoo animal welfare. Instead, the paper is a giraffe-focused paper, useful for giraffes only. In order to be published, I think that the whole idea of the manuscript should be deeply readjusted: the title, the introduction and discussion, etc. For instance, the title should state clearly that the paper presents a selection of important elements for captive giraffe welfare appropriately reviewed and with suggested practical implications.
Thank you for the comments. I am sorry that the manuscript is confusing. It has never been intended that this article is a toolkit for assessing welfare, but it aims to distil down an evidence-based approach to identifying species specific needs. There is no tool or method included in the paper as that was never an intention. Instead, there are seven indicators of welfare that could be assessed. I made sure in Section 3 (line 147) to state this paper aims to catalyse development of the toolkit for giraffe welfare assessment that you mention in your feedback. And the next logical step is for zoos to validate how they should do this based on better knowledge of key giraffe welfare indicators. I have reviewed the paper to ensure any words or phrases that suggest a toolkit or similar are removed and rewritten. I hope it is now clear as to what is general and what is the specific example.
I do believe that the giraffe is a worked example in this paper and I apologise if this has not been made clear. Because the aim of the paper is to show how we can look at fundamental needs for each and every species that we keep, and why such fundamental needs must form part of essential care. This is what is outlined in the introduction. The giraffe is the example to show the application of the evidence based approach for others to follow and check with other species. I have clarified the title accordingly. Once again, I apologise for any confusion regarding the key aims of the manuscript.
I think author should take the current version of the manuscript as the basis for a future paper, but going much further in both directions: A) expandung the connection (justification) of his recommendations based on the natural feeding, habitat and behaviour of giraffes, as well as based on their anatomy, physiology, etc. (I miss information about the "ideal" amount of time a giraffe should be performing feeding behaviours, or the ideal amount of leaves or browse, or the specific nutritional requirements of the species, etc.); and B) detailing the practical information provided. With specific numbers, recommendations, suggested indicators to use, etc. making this paper really useful for zoo staff.
I have some other comments, suggestions and questions. I hope they could help the author to improve his research and to generate valid, reliable, nhew and useful knowledge.
Thank you for the comments and feedback. I have attempted to answer all points and to include relevant extra information in the text. As this is an attempt to illustrate what can indicate good welfare from a behaviour and behavioural expression (i.e. fifth domain) approach, I have not reviewed a manual of how to provide husbandry (i.e. the actual amounts that giraffe should be fed) to be illustrate the outputs that are associated with good care. I have included a statement around following current best practice on diet, housing and daily care and that this seven-step list of welfare identifiers is built on this. There is new information, and reworking, across all sections, including new subheadings in the discussion to add clarity and a logical flow to the evaluation of key concepts.
ABSTRACT and INTRODUCTION
The info in the abstract and the introduction (and description of the aim of the paper) are slightly different (in the abstract the specificities of giraffes are mentioned -the WELFARE, etc., and seems to be more important, while in the introduction it seems that the giraffe is “just” an example. I think this is not the case. As mentioned previously, the tension between the introduction (the aims) and what the paper really is confuses me. In the aims seems that the paper provides a framework that is easily applied to several species, that is a “way to connect theory of welfare and knowledge of the biology of the species and daily caring routines”, with the giraffe as a simple example. However, later on the text is very focused on giraffes and it is not clear what were the processes to identify or create the “WELFARE list” for other species.
Thank you for the comment. I have attempted to edit the abstract and the introduction to ensure there is better explanation of what the paper is examining. I.e. we can identify key welfare identifiers and outputs from our knowledge of species’ needs, here’s an example of what is meant by this using the giraffe. I apologise for any apparent confusing messages in the paper and I hope my edits clarify. I have also re-worked the discussion to explain the general concepts on welfare-focussed husbandry, and the specific worked example of the giraffe.
LINE 19: The idea of using the word WELFARE as a mnemonic tool to remember the presented elements or attributes to work on can be practical for zoo staff, but it can be a little bit confusing because the concept of “welfare” is already central for the proposed WELFARE, and then, the use of the word “welfare” is meaning two (already) connected things (the animal bell-being and the list of important attributes to check) that, however, are not the same. I suggest adding some differentiation in the text. Things such as using W-E-L-F-A-R-E or W.E.L.F.A.R.E, or g-WELFARE or similar.
Edited. Thank you for the feedback and suggestion.
SECTION 2.
LINES 97 -102: Serious doubts about it. And actually a dangerous statement. This sentence can led to the misunderstanding than providing the possibility to express consummatory phase is enough for fulfil all the behavioural needs (controversial but practical concept to use here) related to appetitive behaviour. Many examples (from exploring and foraging in tigers - 10.3390/ani10091536- to rooting in pigs -e.g. Broom and Jorhnson, 2019-) prove that this is not true, and that other behaviours related to feeding can be very important for the welfare, regardless of whether the animals are satiated at the end of the consummatory phase.
Thank you for the comments. I read the papers provided in the reviewer’s feedback and edited this section.
FIGURE 1: It seems interesting, but everything is too vague and general to be useful. How are these three points connected? What should readers “do” with the literature published about the anatomy and physiology of an species? What to look for? Is there any criteria to help navigating through all this literature? How do you consider and/or measure these aspects? What is exactly "measuring appetitive behaviour" for instance? Is this about time invested in? It is about frequency? You mention appetitive behaviour. But is this scheme useful for identifying other important behaviours?
Thank you for the comment. Apologies that figure citation in the text was missing. This has been rectified. I have added more interpretation to the figure citation to provide instruction on its use.
LINES 120: “is not always achievable”. Seems to be "impossible". I suggest replacing it by "is not usually achieved" or "easily achievable" or adding a reference supporting the statement that is not achievable.
Thank you for the comment. This has been edited accordingly.
LINE 131: cause?
Edited
SECTION 3.
LINES 132-135: Where does this selection of issues come from? Do you have any reference of why these aspects are important, or any that support that the current management is solving these issues (care manuals or standards and guidelines, etc.)?
Thank you for the feedback. References provided.
LINE 152: How is the giraffe WELFARE concept specifically helping training in giraffe behaviour? Maybe for giraffe care training...
Edited
LINES 155-157: it is not clear how this simplification and definitions of the core components and needs can be done. The author presents an example, already introduced by Hickey et al., so if giraffe is a species used as an example, it means that this can be applied (at some extent) to other species. How are the processes to actually define the core components and needs of a particular species? There is no information about them in the whole manuscript.
Thank you for the comment. I have expanded on the wider concept of identifying species needs, using dialogue, group discussion, collaboration and embedding stakeholder knowledge and experiences in the Introduction.
LINES 159-163: To me, this is the real outcome of the presented project. It is valuable enough and it probably deserves to be published, but the project does not go further than presenting a practical and scientifically-grounded checklist of critical elements for giraffe welfare protection and promotion.
Thank you for the useful feedback. The aim of the paper is to encourage this approach to become more widespread, with identification of such key “in zoo needs” to be expanded across species and be presented in a way that allows keepers, practitioners, etc. to understand specific welfare needs.
FIGURE 2. I think that the pictures in this figure should be larger, considering that they provide visual information of examples about important aspects (not only beautiful or contextual). I also think that whether different pictures provide visual examples of different welfare indicators, they could be individually identified (each picture with a letter or number associated to the positive or negative specific indicator). I suggest the author to put the letters (WELFARE) in horizontal, with each letter (welfare-related element) associated to each picture (or pictures) placed above or below...
Thank you for the comment. I have uploaded a larger size file with the original submission and have increased the text size further. I have added further explanation to the figure caption of each photo. And each image in the figure is numbered.
WARMTH SECTION: Despite some specific details are shown here (such as the fact that giraffes can die when exposed to <6ºC) and specific recommendations are shown in the table 1 (always >18ºC), I think that this paper (that claims the use of practical info about the giraffe as an example) is lacking some more detailed and practical information. The use of terminology such as "appropriate" is very dependant on each individual perception and should be replaced, when possible, with more rigorous and clear terms. Specifically, when talking about easy-to-measure elements, such as temperature. For example: what is "an adequate external temperature for outside access" in terms of ºC? Do we have scientific literature about temperature ranges of comfort in giraffes? What are the most evidence-based guidelines say about it?
Thank you for the feedback. The need for warmth is taken from two sources, Potter & Clauss (2005) and the EAZA guidelines. The EAZA guidelines are those which are also used by the BIAZA Ungulate Working Group’s Giraffe Focus Group to explain the need for temperatures no less than 18oC and therefore the claims in this article are evidence based. I hope this clarifies your concerns.
ENRICHMENT SECTION: I miss some interesting and practical information, here. The importance of some type of enrichment seems to be clear. But what are the types of enrichment proved to work with giraffes? How tall they should be? What is "an appropriate social" group? In some species, one should expect almost an absolute absence of social conflicts, while in other one should expect certain conflicts without lesions or isolation, etc. What kind of feeders are better, why? I really miss more practical information. Without more detailed information, the giraffe WELFARE checklist is in a no man's land. It is no a deep literature review of the needs of giraffes nor a theoretical complete protocol for giraffe welfare assessment. But in the other hand, it is not detailed enough to be an updated guideline for giraffe care, with very practical information that could be easily followed by a zoo staff in the implementations of actions to improve giraffe welfare.
Thank you for the feedback. The idea behind this paper is not for it to be a husbandry guidelines, but for keepers to identify and understand that enrichment is needed. Keepers have a wealth of resources at their disposal to design and implement enrichment from. This section is clearly referenced with examples of what constitutes giraffe enrichment and what should be considered essential daily husbandry (i.e. browse). Further references to enrichment repositories are included. I hope this clarifies these examples and ideas.
Encompassing under the same concept ("Enrichment") elements related to the collection plan and population management (social group), elements related to the daily management and care routines (using certain type of feeders, etc.), and elements related to facility design (the view across the paddock) seems to be a little bit "forced".
Thank you for the comment. I’m sorry that you find this section forced. Social enrichment is a form of enrichment (Bloomsmith et al., 1991) as it allows animals choices as to who to associate with and spend their time social or solitary accordingly. The wealth of research on giraffe social structure that has emerged in the last few years shows the importance of social choice to their welfare, and therefore lives in captivity are enriched when social structure considers individual choices. A further reference has been included.
LINES 186-187: How do you suggest merging these two aspects? With a certain minimum facility surface? With design elements (barriers or other separations)?
My apologies, I am confused by this comment. Is this relating to social group size or to providing enrichment that increases interest in the environment? If the reviewer could clarify that would be helpful. Thank you.
LINE 189: I would say that enrichment is necessary and important always (some outside facilities can provide very low opportunities to express natural feeding behaviours without enrichment).
Edited.
LEAVES: In comparison to Warmth and Enrichment, this section is much clearer and more practical (although the ideal amount of leaves/browse might be stated, even if very hard to achieve). What should be the ideal? is there any "minimum amount" to guarantee an adequate giraffes' endocrine and/or gastrointestinal health?
Thank you for the comment. I have provided review of what should be provided (as a percentage of total intake) from leaves/browse in the paper.
FEEDING:
LINE 219: Related to “at a several times per day”. Any recommendation? Several times could mean two or twenty depending on the reader. Is there any study recommending a minimum number of takes? Shall it be distributed along all day or during specific periods of time (day? night? etc.)? If this interesting manuscript tries to create something practical and based on natural history of giraffes, providing information regarding their activity budget and their daily biological rhythms could be very useful here.
Thank you for the comment. I have linked back to available husbandry guidelines and suggested that captive foraging should follow wild patterns of feeding activity.
Finding in "Rumination" information that would help the reader to understand how to be good in the "Feeding" section is not practical.
Thank you for comment. I am not sure of the instruction here but I have rationalised the rumination section all the same.
LINES 2019-220: Why are not specified in the present paper (referencing EAZA and other good guidelines)? According to the author, one of the manuscript’s aims is "iii) to move away from theoretical review of welfare definitions to encourage practitioners and animal care staff to look at their species". But this seems week when the recommendation is as simple as "Concentrate rations should be fed in weighed amounts for each individual animal in 215 the herd, at several times per day [...]". As mentioned before, I think author should take the current version of the manuscript as the basis for a future paper, but going much further in both directions: its connection with basic knowledge to identify giraffe needs and wants based on evolutionary ecology, anatomy and physiology, and behaviour, etc. and also making the manuscript much more detailed in requirements or recommendations (specific temperature degrees, expected amount of time ruminating, expected amount of leaves or browse, enrichment devices detailed, etc.).
Thank you for the feedback. I am not sure what the direction or instruction is here. If the reviewer could provide more clarity that would be useful. I have not stated the volume of food given as there are husbandry manuals provided for this, and I am not critiquing or reviewing these instructions (which are good). I am explaining what keepers need to do to provide a foundation for their giraffes to experience good welfare.
Exercise: Aren't these, part of the enrichment goals?
Thank you for the question. I have included exercise as a separate category to promote physical health and condition, and foot health. And to ensure that simply a large open space was not something that was considered enough to occupy an animal. As giraffes like to wander, they should have the ability to do this in a suitable enclosure.
LINE 250: are (instead of is)?
Edited
TABLE 1: In general, the table lists interesting aspects related to giraffe welfare, but the provision of information to facilitate an adequate answer is vague, affecting negatively one of the aims of the present manuscript, which is to create something practical. The Table 1 provides a list of potentially relevant welfare questions, but the provision of references that help zoo staff answering the suggested questions is not consistent.
Thank you for the feedback. I have attempted to revise the referencing and use of examples in the table.
In relation to warmth, there is the info related to >18ºC for indoor temperature (this is, to me, the example of what this giraffe WELFARE should look like. A place with justified specific references and recommendations that are important for welfare. Why there are no a minimum outside temperature? Is there any factor related to giraffes’ thermal comfort that changes between outside and inside (for instance, what can giraffes do to thermoregulate while outside?). Why does author not simply ask for ensuring that the giraffes are always >18ºC no matter where they are? Any explanation?
I am afraid I cannot answer this question. Husbandry guidelines state that animals should be given indoor access when temperatures fall below 18 degrees. Further research, that I have included, shows that low (single figure) temperatures cause undue physiological stress and therefore must be avoided. I have simply reviewed the available information.
Related to enrichment: How does the author suggest assessing interest and engagement? it is a matter of using an ethogram and/or about investing a certain amount of time? What should be looked for? In relation to autonomy, If the author does not specify more, this question is tricky from a practical point of view. I can imagine many people being able to justify a YES and a NO for the same giraffe in relation to this point. The importance of choice and control for animal welfare is clear. And it is great that the author points it here. But "some" is a complex and subjective concept. One can say that the animal can go to the door of the facility and to the other extreme of the internal facility, or that the giraffe can sleep and move and smell, so this is "some" (enough) self-control over what they do. Others (like me) would consider that this is NOT ENOUGH degree of autonomy and that welfare issues may arise from this “not enough” degree of autonomy.
Thank you for the feedback. I have edited this section for clarity.
In relation to Leaves: Giraffes should be provided with browse ad libitum?
Thank you for the comment. There is no prescribed amount of browse per giraffe. This was considered in past papers (minimum 25% of daily intake) but this has been shown to be very challenging to impossible (Hatt et al., 2005). I have included these citations in the paper.
In relation to Feeding: That pelleted ration should be provided accordingly to animal weight and needs is obvious and widely accepted. What about placing in the paper the most updated list of nutritional requirements for the species? What about talking about the most common nutritional problems related to pellets (is there any particular element or nutrient in the pellets that tend to be wrongly prepared or calculated? Etc.). Ad “body” before “condition”. And regarding the Figure 2 reference, I think author should cite the specific picture in the figure.
Thank you for the feedback. I have referenced the available husbandry guidelines that are accessible. I would expect keepers to be aware of these and therefore I am simply pointing that correct feeding, based on evidence-based practices is what is needed and diets should be species appropriate. Without the provision of a species appropriate diet, welfare cannot, ever, begin to be good. I appreciate your comments and thoughts here but I am not trying to write a husbandry guideline. I am trying to provide a checklist that could be useful in the zoo based on the evidence that we have at our disposal and why correct feeding, promotion of rumination etc. is needed.
In relation to Rumination: what is “a meaningful amount of time”? Any more objective way to assess it?. More importantly, the concept of “making the best possible efforts” is dangerous. As an informal recommendation, as a talk in a zoo, this might be fine. But as a scientific paper, I think good will is (sadly) not enough. Good will (making the best possible) does not guarantee good welfare in many zoos. I think focusing on "WHAT TO LOOK FOR, WHAT TO DO AND WHY" should be the basis of this paper, and WHAT TO DO or to ensure that all giraffes regularly ruminate each day and/or HOW TO ASSESS IT is what should be stated.
Thank you for the feedback, I have stipulated in the paper the amount of time free-living giraffe have been observed ruminating and I have reiterated this point. I have linked back to Figure 1 in the discussion to provide further context.
- DISCUSSION
Part of the information here is essential to understand the previous section (section 3). I recommend an important restructuration of the manuscript because I think that the scientific justification for the 7 elements of the giraffe WELFARE (from the rationale to the specific suggested requirements) must be placed together.
Thank you for the feedback. The discussion has been reviewed and restructured according to reviewer feedback.
LINES 263-267: Personally, I don't see the conflict between academic debate around theoretical concepts of welfare and the design and implement of best caring practices or guidelines (practice). To my knowledge, they actually benefit each other and, usually, they do not even compete for funding or resources. I would avoid using a non-existent debate between two critical elements of welfare to increase the perception of importance around the creation of practical welfare guidelines or literature.
Thank you for the comment. I was trying to explain that academic theory may be at odds with what is actually needed to move zoo husbandry forwards from a practical perspective. I.e. it is great to know what emotional states are on paper, but how can we identify them when the animal is in front of us. I have edited this section accordingly.
LINES 280-281: The relationship between food quality and the affective state is not so direct. To my knowledge, welfare is not a binary concept but a continuous and gradual one. This means that poor-quality forage, and especially inappropriate forage, yes, they can have negative impact in the welfare of a giraffe, but experiencing a positive mental output is affected by many other factors (see the Five Domains Modell, for example: 10.3390/ani10101870).
Thank you for the comment. I haven’t suggested welfare is binary but poor quality forage, and a lack of palatability causing a reduction in forage intake and therefore increases chances of behavioural problems and pathology is noted in the literature. Ruminant health and welfare is intertwined with the ability to forage and ruminate. I have included a citation and edited the sentence accordingly.
TABLE 2: Especially the selection of the indicators, should be more specified and justified using references that connect the suggested indicators with the specific attribute aimed to evaluate.
Regarding warmth and enhanced longevity: Is this a valid indicator for warmth? the paper from Bercovitch and colleague does not test it. Problems with environmental temperature can reduce longevity, as problems with feeding, health care, stress... The connection between longevity and the attribute (Warmth) should be detailed.
I am not familiar with the Bercovitch paper that the reviewer refers to here. I am familiar with this author’s work on wild giraffe. In captivity, it is clear, prolonged cold kills giraffe. The evidence for this is substantiated and factored into husbandry guidelines (e.g. EAZA) and available in papers such as Potter & Clauss 2005.
Also, how is warmth related to the promotion of rumination? Please add a reference.
Please the title of the table, that MAY form the basis of measurement of the fifth domain. I have not referenced this column because I am posing ideas for people to go and test and measure. Nobody has measured the mental state of giraffe yet. I am encouraging them to do it. I have included rumination aligned with comfort because when ruminants are comfortable, they will ruminate more (e.g. Baxter & Plowman, 2001).
TABLE S1 (Line 300): In my opinion, Table S1 is important enough (and small enough) to be included in the main manuscript. Moreover, the table could be expanded with a description of the important elements seen in the videos or what to pay attention to (for instance, describing the characteristics that a feeder should have to increase foraging -feeding- time, what to look when assessing rumination and how to measure/record it, etc.).
Thank you for the comment. I am pleased that you find this useful. I have included further description in the comment for each video and it is now included in the main text.
LINE 301: “Once captive giraffes are provided with WELFARE”… the problem is that, in the present manuscript, there is no way to know whether a certain facility is providing WELFARE or not to the giraffes because it is not clear when and how to ensure that the 7-ítems list is enough followed or achieved. The lack of validated indicators correctly placed in each attribute, the lack of specific information to follow to understand whether enrichment, warmth, leaves, etc. are provided in ENOUGH quality and/or quantity, this makes the connection between WELFARE and the real welfare (the fifth domain) weak or vague. To me, one of the weaknesses of the manuscript is that it is a little contradictory that the manuscript is (to me, correctly) advocating for welfare-focused husbandry, for knowing the species in deep, for using evidence-based knowledge to improve giraffe care, etc. but at the same time, the manuscript is presenting a justified but vague checking list of elements or questions, without details on how or in which degree to achieve them, or how to assess them (even if they are focused on welfare indicators related to the four physical domains).
Thank you for your feedback and comment. I am sorry that you feel this part of the manuscript is vague. I have edited this comment to show that such an approach should be validated and then further review and assessment of the fifth domain may be possible. As we have very little information at present on what any measurement of the fifth domain may be like for zoo animals, and yet it is going to be an expectation of welfare assessment in the near future (if not already), I have attempted to suggest (not prescribe) a way that this could be done. I feel that this, in itself, is useful in helping others develop structured and validated tools.
Lines 326-328: I think that, unfortunately, the current status of the manuscript does not allow the author to conclude this. There is not enough novel information, the rationale behind the WELFARE elements could be expanded and explored deeper (as well as their connection to giraffe biology and ecology), and the manuscript does not provide enough detailed information that can be followed to fulfil the needs related to the seven-step WELFARE elements or to assess if giraffe caring is successful or not.
Thank you for the feedback. I respectfully disagree. Each section of W-E-L-F-A-R-E has scientific evidence embedded into it. Each section is thoroughly referenced and identifies the priorities that should be the focus of what giraffes need, as a baseline. I have been at pains to explain that this work should be a foundation for further validation if developed into a welfare toolkit and I believe that the evidence in the paper supports why fundamental giraffe husbandry needs to consider these seven steps. Please note that as the discussion has been re-written and re-structured this has now been moved in a more evaluative and discursive section of the paper.
LINE 361: But the paper does not provide clear information about how the use of this knowledge (on evolutionary ecology, anatomy and physiology, and behaviour of giraffes) helps the identification of giraffes' needs. Instead, it is the "classic" literature review, mostly based on (excellent) published papers on giraffe care, what has been done to support all the giraffe WELFARE proposal. To me, using this literature is good, but the paper does not create or show how to identify species-specific needs from the evolutionary ecology, anatomy, physiology, and behaviour of a particular species
Thank you for the comments and useful feedback. I am extremely grateful for the thorough review of the subject area. I hope the edits to the paper make it clearer and more applicable.
