Changes in the Stress Tolerance of Dwarf Rabbits in Animal-Assisted Interventions
Round 1
Reviewer 1 Report
The manuscript tells a complete story and the research is interesting to
the reader. However, some misunderstandings and puzzles are listed below
that require explanation or basic details.
1. In the "Master Method Test" and "Child Method Test", the rabbit's 12
tasks and 8 tasks should be clearly listed so that the reader can
understand all the tests.
2. As the authors say, "Rabbits earn additional 'bonus' points based on
their response time (latency) to situations: Evaluation of response
times in situations 1-6 and 10-12", the authors can explain in detail
why these situations are worthwhile Additional 'bonus' points or not
otherwise.
3. Need to be described in more detail, for example, the authors could
clearly describe the scoring rules in the Owner's Method Test.
Author Response
First reviewer -
- In the "Master Method Test" and "Child Method Test", the rabbit's 12 tasks and 8 tasks should be clearly listed so that the reader can understand all the tests.
APPENDIX A (Owner Approach Test) and B (Children Approach Test) are added to the article.
LINE appendix A 451-556
LINE appendix B 559-611
- As the authors say, "Rabbits earn additional 'bonus' points based on their response time (latency) to situations: Evaluation of response times in situations 1-6 and 10-12", the authors can explain in detail why these situations are worthwhile Additional 'bonus' points or not otherwise.
Extended the article with the answer in line: 256-261
- Need to be described in more detail, for example, the authors could clearly describe the scoring rules in the Owner's Method Test.
Extended the “Materials and Methods” section in the article
Line: 200-206 and 245-261
Reviewer 2 Report
The paper presents the results of a research carried out on 20 dwarf rabbits. The rabbits were the progeny of a single buck mated to three does. Four of them had previously received handling during the sensitive period after birth. The age, sex and reproductive status of rabbits are not reported.
The number of animals handled appears to be too small to allow a comparison with those not handled. It is not specified what type of manipulation these animals received. Also the consanguinity of the subjects does not allow to obtain results of a general nature.
The manipulations by the children to which the rabbits have been subjected, in my opinion, are to be considered excessive and dangerous for the animal's well-being, especially when the animal is kept off the ground, as in figure 2b. A poor reactivity of the animal to stimuli can be the result of a phenomenon of learned helplessness, indicating an even greater stress for the animal
It is also unclear who assessed the rabbit behavior with the owner and the child in the two tests. Was the behavior assessed directly or by analyzing test videos? By one person? With what ethological preparation?
On line 205, the sentence: "After that the owner took the rabbit out of the cage and kept stroking it by placing it in their lap and then held the animal in their hands", has a grammatical error.
In the conclusion, the authors write: "That means those rabbit breeders who are raising for therapy usage reason, need to undertake the kits to the sensitization of human hands' touch." I think they mean habituation and not sensitization which is the exact opposite.
For all these reasons I believe that the paper has little scientific value and cannot be accepted for publication. Furthermore, the argument has nothing to do with the title of the special issue "Animal Behavior in Intensive Culture Environment".
Author Response
Second reviewer
The number of animals handled appears to be too small to allow a comparison with those not handled.
Originally we started a larger sample size but unfortunately this size was lowered due to other reasons.
- It is not specified what type of manipulation these animals received.
Extended the “Materials and Methods” section in the article with the handling method from line 164-168
- Also the consanguinity of the subjects does not allow to obtain results of a general nature.
We admit that the analyzed group of rabbits consisted of full and half-sibs, respectively.
- The manipulations by the children to which the rabbits have been subjected, in my opinion, are to be considered excessive and dangerous for the animal's well-being, especially when the animal is kept off the ground, as in figure 2b.
Extended the “Materials and Methods” section in the article with expressing that the children worked in pairs WITH the assistance of a camp supervisor who were all previously informed about the methodology and prepared to the animal assisted interventions.
Line: 288-292
- A poor reactivity of the animal to stimuli can be the result of a phenomenon of learned helplessness, indicating an even greater stress for the animal
Those animals whose behavior was passive during the interventions received higher points than those who were trying to escape although the passive ones reached less scores than those rabbits who were friendly, curious and were looking for the company of the testing person. To clearly separate the moveless (freezing down) rabbit that shows signs of fear from the rabbit that does not show any interest (staying passive during the activity) by for example the rabbit’s ears position, behavior is obvious for a specialist (PhD in ethology topic).
line: 200-209
- It is also unclear who assessed the rabbit behavior with the owner and the child in the two tests.
The assistant during the human approach tests was the third author who does not have preliminary contact with the rabbits (independent person).
Line: 206-209
- Was the behavior assessed directly or by analyzing test videos?
The behavior was assisted directly.
line: 209
- By one person?
OAT and CAT test was assisted by one person, the third author (Professional, PhD ethology topic) who did not have preliminary contact with the rabbits (independent person).
Line: 206-207
- With what ethological preparation?
Professional, PhD ethology specialization (Line 206-207)
- On line 205, the sentence: "After that the owner took the rabbit out of the cage and kept stroking it by placing it in their lap and then held the animal in their hands", has a grammatical error.
Sentence had been corrected. Line: 237-239
„After that the owner took the rabbit out from the cage and placing it in their lap and kept stroking it. 15 seconds later stood up with the animal in their hands and kept stroking.”
Line: 237-239
- In the conclusion, the authors write:
"That means those rabbit breeders who are raising for therapy usage reason, need to undertake the kits to the sensitization of human hands' touch."
I think they mean habituation and not sensitization which is the exact opposite.
The sentence had been corrected.
Thus, rabbits which are intended to be used for animal-assisted interventions are strongly recommended to undergo handling during their sensitive period after birth as the rabbits receiving handling show measurably higher interest and cooperation.
Line: 439-442
For all these reasons I believe that the paper has little scientific value and cannot be accepted for publication.
Furthermore, the argument has nothing to do with the title of the special issue "Animal Behavior in Intensive Culture Environment".
Reviewer 3 Report
The manuscript “Changes in the stress tolerance of dwarf rabbits in animal assisted interventions “is very interesting. The literature on the use of rabbits in AAI is limited and this paper appears to be a major development in the field, the findings are useful to assess the number of the sessions in order to limit stress levels of involved animals and to use preferentially subjects that have been previosly handled during the nursing period.
Specific comments:
- Abstracts generally do not contain references, so I recommend deleting it.
- The conclusion regarding the use of rabbits in AAI for a maximum of two sessions should be included in the abstract
- Line 39: In AAI the species more used are dogs, cats, rabbits, donkeys and horses... please add some references.
-Line 40: I would modify this sentence: In therapy programmes 28% rabbits, 15% small mammals and 10% birds are being used... I would prefer a list where the sum of the percentages is 100. Furthermore rabbits are small mammals... I think a better description is needed
- Line 43: I suggest to include some examples on how to understand rabbit’s body language
- Line 126 and 146: replace, please, “subjects” with “groups” and “result” with “study”
- Line 152: Mean age and weight of dwarf rabbits should be included.
- Line 154: in literature there are no data on early handling in dwarf rabbits. A short description of sensitive period, age and duration of handling treatment is mandatory.
- I think it could be better here to add that rabbits were considered to belong to two different groups: Subjects that had previously received handling during the sensitive period after birth (n.4 Group H) and subjects without handling experience during the sensitive period after birth (n.16 Group NH)
- Linee 232 Add reference
- Table 2: Add “Table 2” in the caption. I believe that for the purpose of the study, the rabbits can be numbered from 1 to 20. Asterisks 1 and 2 are not needed in table 2 and 3.
- I would see an asterisk and the P value in the figure 3 (a) and in figure 4 (a).
- Line 329 No explicative this sentence “For the third intervention the difference between the two groups dropped to 4.15% (for the good of the handled group)” rephrase!
The explanation of results in the Discussion is poor I would like to find an interpretation of results more detailed and with references. It is possible to add more references related this Species? Limitation of the study should be included.
Author Response
3rd Reviewer
Comments and Suggestions for Authors
The manuscript “Changes in the stress tolerance of dwarf rabbits in animal assisted interventions “is very interesting.
The literature on the use of rabbits in AAI is limited and this paper appears to be a major development in the field, the findings are useful to assess the number of the sessions in order to limit stress levels of involved animals and to use preferentially subjects that have been previosly handled during the nursing period.
Specific comments:
- - Abstracts generally do not contain references, so I recommend deleting it.
Corrected
- - The conclusion regarding the use of rabbits in AAI for a maximum of two sessions should be included in the abstract.
Added to the abstract
Line 22-23 and Line 25-26
- - Line 39: In AAI the species more used are dogs, cats, rabbits, donkeys and horses... please add some references.
Added
Line 42
- -Line 40: I would modify this sentence: In therapy programmes 28% rabbits, 15% small mammals and 10% birds are being used... I would prefer a list where the sum of the percentages is 100. Furthermore rabbits are small mammals... I think a better description is needed
Modified
Line: 42-43
- - Line 43: I suggest to include some examples on how to understand rabbit’s body language
Modified:
Line 46-51, extended and added a new reference
- - Line 126 and 146: replace, please, “subjects” with “groups” and “result” with “study”
Replaced the words
Line 135 and 144
- - Line 152: Mean age and weight of dwarf rabbits should be included.
Added
Line:
163-164
- - Line 154: in literature there are no data on early handling in dwarf rabbits. A short description of sensitive period, age and duration of handling treatment is mandatory. - I think it could be better here to add that rabbits were considered to belong to two different groups: Subjects that had previously received handling during the sensitive period after birth (n.4 Group H) and subjects without handling experience during the sensitive period after birth (n.16 Group NH)
Modified
Line: 164-168
- - Line 232 Add reference
Done
Line: 296
- - Table 2: Add “Table 2” in the caption. I believe that for the purpose of the study, the rabbits can be numbered from 1 to 20. Asterisks 1 and 2 are not needed in table 2 and 3.
Made all the changes
Line: 342
- - I would see an asterisk and the P value in the figure 3 (a) and in figure 4 (a).
Corrected
- - Line 329 No explicative this sentence “For the third intervention the difference between the two groups dropped to 4.15% (for the good of the handled group)” rephrase!
Sentence rewritten
Line: 399-402
- The explanation of results in the Discussion is poor I would like to find an interpretation of results more detailed and with references. It is possible to add more references related this Species?
Corrected
- Limitation of the study should be included.
Limitation of our study: To determine the stress level of the rabbits by behavior examination is not exact although it gives us clear information and the test were fulfilled by a specialist (PhD in ethology topic). To have accurate data parallel with the behavior examination hormone of control is reasonable to determine. Our tests could be verified by defining cortisol hormone level.
Line: 436-441
Reviewer 4 Report
Please see the attached document.
Comments for author File: 
Comments.docx
Author Response
4th reviewer
Notes for authors Dear Authors,
Thank you for your paper, which aims to explore the stress experienced by dwarf rabbits involved in a children’s animal assisted intervention (AAI) programme. I commend your choice of topic, as it is not often that rabbits are discussed in the context of animal assisted interventions. In addition, for ethical and animal welfare reasons, it is essential that the responses of any AAI participants (including rabbits) are appropriately monitored and interpreted.
Your introduction is good, although some of the English language and/or terminology could be improved, and it could be more explicit about the gaps in the literature and how your research seeks to address them.
However, I have concerns about the research design and/or reporting and believe that the paper itself is also somewhat underdeveloped.
Firstly, I could not find any reference to this project’s ethical approvals.
I would expect that you received (prior) ethical approval from a relevant animal research ethics committee (AREC) for the involvement of the rabbits, and (prior) approval from a human research ethics committee (HREC) for the children’s involvement in the study.
I note that 20 rabbits were involved.
Did these belong to just one owner or multiple owners? – YES, Line: 168
Did their owner(s) provide informed consent for their participation in the research.
If so, how (written, oral)? Not needed, all of them are owned by the first author
Did the parents of the children involved also provide informed consent for their participation? If so, how? YES, written, with the allowance of making photos and videos. Line: 270-274
I expect that this may be especially important as the AAI was run for children under the care of the Child and Family Protection service, and so they may have been especially vulnerable.
Ethical approvals and informed consent should be described in the paper.
How did you protect the welfare of the rabbits during the interventions?
The assistant and the supervisor of the AAI were specialist of animal,
In particular, how did you ensure that the children handled the rabbits appropriately and did not risk dropping them? previously educated the camp counselors and the test assistant (PhD ethology topic) and the owner of the rabbit (1st author, PhD student ethology topic) were controlling the AAI
Line: 266-269, 275-284
This is particularly important, as inappropriate handling can result in vertebral fractures in rabbits and this condition could warrant euthanasia.
What happened if a rabbit displayed fear or aggression during an intervention?
Aggression did not happened, rabbits who showed signs of fear got less point of course and let them to relax in their cage.
Did you remove him/her from participation or give them a break?
It was not necessary to remove any animal.
If this was not an issue, did you have a plan for this anyway?
In case of aggression or signs of exhaustion the rabbit would have been removed and given a calm environment in its cage.
Secondly, with regard to the experimental design/materials and methods section, many questions have been left unanswered.
What was your hypothesis?
Fitted to the article
LINE: 224-229
What were the goals for the children involved in the intervention/what was the purpose of the AAI?
Added to the article
LINE: 286-288
Why did you use an approach test as a proxy for the rabbits’ stress levels?
Because rabbits body language is easy to read for specialist (ethology) and rabbit breeders). We were ready to interrupt if needed but this not happened. Our rabbits are selected for tameness during six generations.
What was the significance of the owner approach test? 0.05
Why did you decide not to use more conventional animal welfare indicators such as behavioural and physiological signs of stress (e.g. cortisol, heart rate etc.)?
As the continuation of our research we had already begun collecting samples to measure level of cortisol. Blood sampling is straining for the animal in itself, more stressful than AAI. Sampling from saliva does not always work in case of rabbits because to properly insert the sampling wand into the rabbit's mouth is difficult. Therefore, we chose to sample faeces because 24 hours after the stress, cortisol metabolites can be determined in laboratory. We are collecting samples in normal condition (the site of the animal 1 day before the AAI, ad libitum water/hay and feeding twice a day: in the morning 7 AM and 12 hours later), and then after stress, 24 hours after the AAI. We are interested in the difference / change, not just the absolute value.
Among the devices that can be used for heart rate measurement:
- the use of belts with external sensors can be confusing during AAI not only for the animals but also for the children,
- implanted surgically pulse detector’s prize is very high.
Approach or latency to approach alone does not provide much information about a rabbit’s stress level or emotional state.
For example, a rabbit could approach a human out of interest/curiosity or joy/play, or to display fear- motivated aggression.
Alternatively, a rabbit may fail to approach a person (or approach them more slowly) due to fear, lack of interest, engagement in other activities, or habituation.
To clearly separate the moveless (freezing down) rabbit that shows signs of fear from the rabbit that does not show any interest (staying passive during the activity) by for example the rabbit’s ears position, behavior is obvious for a specialist (PhD in ethology topic).
LINE 203-207
What were the approach tests and scoring system modelled on?
Previous research projects/papers by other authors? If so, you will need to include this information. If not, what was your rationale for the approach and how did you design the scoring system?
Overall, the scoring system was very unclear and requires further explanation.
Who performed the scoring?
Detailed methodology of both tests were provided in Appendix.
In these tests the consecutive tasks were formed resulting an increasing pressure on the animals.
An independent observer using formal behaviour observation methods?
Yes
Was an ethogram used to identify the signs of stress and/or fear and aggression (anger)?
If so, please include it and describe key aspects in the text.
No, the assistant could understand the rabbit’s behaviour.
How were the rabbits transported to the location? LINE: 274-280
How many sessions did each rabbit participate in? LINE: 300-302
Exactly how many times was each rabbit handled? LINE: 300-302
I think that you included the latter two points but I could not decipher them.
Overall, I would not be able to fully replicate your experiments using the information provided in your methodology.
I must also add that the face of the child in Figure 2b is not sufficiently blurred and she would still be identifiable from the image.
The total blurring is not necessary as written allowance of using the photos was given by the parents.
You may also wish to enhance the blurring in Figure 1. The total blurring is not necessary
The data in your results section are reported concisely and clearly presented in the tables and figures.
Table 2 needs to be titled/labelled.
The title added.
Line: 342
Without understanding the scoring system, however, it is difficult to interpret your findings. Was the maximum possible approach score 100?
NO! Line: 263
Therefore the % reduction in approach scores were calculated by dividing by 100 rather than by dividing the amount of reduction by the first approach score and multiplying by 100?
NO!
You used the mean to report central tendency.
Were the data normally distributed?
What statistical test did you use to determine this?
Normality was not tested because we used the PROC MIXED where the calculation was based on REML.
Only four rabbits had not received handling during their sensitive period, so this limits the conclusions that can be drawn about how prior handling experience may benefit AAI.
Your discussion section needs to be more developed and you will need to put your findings in the context of contemporary literature.
You will also need to discuss the limitations of your study and to suggest future directions for research.
Line: 436-441
Your conclusions section is currently too long.
This section is normally reserved for your main “take home messages”.
A single short paragraph would usually suffice.
Rewritten
Line: 442-452
Please see below for some additional comments.
Once again, thank you for your submission, and I hope that my feedback comments are helpful.
Specific comments:
- Lines 82-84 (Introduction): “Certain specific stimuli trigger learning pro- cesses, which influence the behaviour of the individuals for the rest of their lives, i.e. there is a sensitive period for imprinting”. “Socialisation” would be a more suitable term than “imprinting”. Socialisation involves positive interactions with humans. Imprinting refers to identifying the mother/carer immediately or very soon after birth.
Word changed! Line: 91
- Lines 97-101 (Introduction): “Csatádi [18] examined the effects of early handling under laboratory and natural conditions. He used chinchilla rabbits and New Zealand white rabbits in his research. In the laboratory tests, handling, i.e. touching the kits, was carried out during the first week after birth within half an hour following suckling. At these times, the weight of the kits was typically measured and their ears were marked: all this took about 3 to 5 minutes per litter”. What was the result of this? What is the significance of this with regard to your research?
Extended the article. Line: 109-110
- Lines 131-133 (Introduction): “The conclusion of the study is that the carrier cages are a major stressor for the animals, so their confidentiality level decreases significantly.” What does “confidentiality level” mean? Tolerance of handling?
Tolerance of stress
- Line 138 (Introduction): “inclusive primary school” What does this mean?
School where children with special needs also attend (for example ADHD, Asperger Syndrome, Autistic, Dyslexia, Dysgraphia, Dyscalculia etc.)
- Line 139 (Introduction): “first-formers” What age(s) are the children in this class? Grade levels can vary in different countries.
6 and 7 years old.
Line: 148
- Lines 179-180 (Materials and methods): “Veterinary checks were conducted on all rabbits (feces) prior to the animal-assisted sessions, to detect possible health problems.” More details are needed on the veterinary checks. What was involved? A physical/clinical examination and faecal analysis? Dental examination? Blood screening?
The paragraph had been extended
Line: 193-198
- Lines 185 (Materials and methods): “confidentiality” Does this mean tolerance of handling?
By the rabbits confidentiality we can get information about the rabbit’s stress toleration. Appendix A and B helps to follow the method.
- Lines 192 (Materials and methods): “familiarity” What does this mean?
Word modified
Line: 218
- Lines 211-213 (Materials and methods): “The numbers of the responses listed under each aspect (1-12) also represents the point value with a higher score increasing in line with the expected behavior. In parallel, the animal’s response latency was also measured.” How was this calculated and/or assigned? More details are needed.
Details are given.
Line: 145-155
- Lines 213-214 (Materials and methods): “For each activity, the behavioral response was being observed..” Who made the observations and what process was used to observe and record this?
Line: 205 and 246
- Lines 215-216 (Materials and methods): “The rabbits received additional ‘bonus’ points depending on their response time measured in seconds (latency) to the situations” How was this calculated?
Line: 260
- Line 223 (Materials and methods): “transport” More details are needed on transport and how rabbit welfare was safeguarded during transport, handling by staff and children, and within the whole AAI.
Line: 266-280 an 288-292
- Lines 227-228 (Materials and methods: “Each rabbit was handled by two children at a time assisted by a teacher/camp counsellor.” Increased clarity needed on the total number of times each rabbit was handled (and total duration of handling) and the total number of children that handled each rabbit.
Line: 300-302
- Line 250 (Materials and methods) Who performed the observations and how did they do this?
The third author was responsible for the data recording the first author was responsible for animal welfare and the camp attendants were responsible for children safety
- Line 262 (Results): Please refer to my commentary & please see additional remarks below Please clarify the terms “confidentiality”, “Dinamical confidentiality deficit”, “diminution” (does this mean reduction?), and “familiarity”. Please provide additional explanation on how the calculations were made.
Corrected
Please label Table 2.
- Line 334 (Discussion): Please refer to my commentary & please see additional remarks below More discussion is needed.
Your results should be discussed with reference to contemporary literature. Corrected
There seemed to be much individual variation in the rabbits’ response to AAI. This merits discussion, in addition to socialisation at a young age. The limitations of the study must be discussed. Suggest future research directions.
Line: 436-441
- Conclusions: Please refer to my commentary
Round 2
Reviewer 2 Report
kind authors
thank you for your reply but despite the explanations you have made to the paper I believe that serious methodological errors remain and that your paper, in my opinion, cannot be accepted for publication.
Author Response
Authors acknowledge the reviwer's opinion.
Reviewer 3 Report
The manuscript has improved, thanks to the authors for their efforts.
Minor comments:
Line 20: Delete "the first one"
Line 170: Delete "The owner of the rabbits is the first author." This information is useful but it is better to introduce it in another way: Line 233 During the test the owner (Initial letters of the owner's name)...
Line 208: Instead of "All the tests were assisted by one person, the third author (Professional, PhD ethology topic)" I suggest : All the tests were assisted by a PhD in ethology topic (Initial letters of the third author's name) ...
Table 2 and 3: Since the groups are indicated in brackets, I suggest removing the quotes 1 and 2
Figure 3 and Figure 4: I would like to see an asterisk indicating significance
Line 438: The limitation of the study is having taken bibliographic references relating to other species of rabbits. Unfortunately, to the knowledge of the authors, there are no studies on sensitive periods in dwarf rabbits. The non-invasive evaluation of stress hormones in rabbits has also not been sufficiently studied, therefore it cannot be a limitation of this study.
Author Response
Comments and Suggestions for Authors The manuscript has improved, thanks to the authors for their efforts.
Minor comments:
Line 20: Delete "the first one"
Done
Line 170: Delete "The owner of the rabbits is the first author." This information is useful but it is better to introduce it in another way:
Done – Line 222
Line 233 During the test the owner (Initial letters of the owner's name)...
Done
Line 208: Instead of "All the tests were assisted by one person, the third author (Professional, PhD ethology topic)" I suggest : All the tests were assisted by a PhD in ethology topic (Initial letters of the third author's name) ...
Done
Table 2 and 3: Since the groups are indicated in brackets, I suggest removing the quotes
Table 2 Done
Table 3 Done
1 and 2 Figure 3 and Figure 4: I would like to see an asterisk indicating significance
Figures were extended with letters. Means with different letter marks are significantly diverge from each other (p<0.05).
Line 438: The limitation of the study is having taken bibliographic references relating to other species of rabbits.
Unfortunately, to the knowledge of the authors, there are no studies on sensitive periods in dwarf rabbits.
The non-invasive evaluation of stress hormones in rabbits has also not been sufficiently studied, therefore it cannot be a limitation of this study.
Dwarf rabbits are not another species of the rabbits (Oryctolagus cuniculus), therefore they do not differ from the bibliographic referenced examined rabbits.
Reviewer 4 Report
Dear Authors,
Thank you for taking my comments seriously and greatly enhancing your manuscript. I no longer have any ethical concerns about the study. In addition, your methodology and scoring system (and your reasons for using these) are now more transparent and your experiments would be reproducible. The manuscript's English language has also been improved (although further improvements could still be made). However, your discussion still significantly lacks discussion with regard to the literature. I suggest that you discuss your findings in light of some of the literature presented in your introduction. In addition, I recommend reading and referring to d'Ovidio et al. (2010)'Sex differences in human-directed social behaviour in pet rabbits'. Journal of Veterinary Behavior, 15, pp. 37-42 to discuss individual differences & Mullan, S. M. and Main, D.C.J. 'Behaviour and personality of pet rabbits and their interactions with their owners.' The Veterinary Record, 160, pp. 516-520 & Schepers et al. (2009) 'Welfare assessment in pet rabbits' Animal Welfare, 18, pp. 477-485 to discuss the impact of the environment (frequency of handling by the owner and open spaces respectively) on the behaviour of your rabbits. I also recommend some additional slight edits. Change 'imprinting' to 'socialisation' (or 'imprinted' to 'socialised' or 'imprint' to 'socialise') (as appropriate) in lines 15, 21, 22, 129, 348. Add further details about rabbit behaviour signals to your introduction. For example, fearful rabbits can also crouch, have tense musculature, freeze, scan the environment/demonstrate vigilance, attempt to hide or escape, kick/struggle when held, scream, grunt, or thump. Other signs of aggression include charging, biting, and raking with claws. Some additional signs of calmness or relaxation include grooming, lying on the side or abdomen with hind limbs stretched out, and loose ears. Please note that p= 0.02 was given in the caption for Figure 4 but not reported in the text. Overall, it is now clear that your research definitely has merit and should be published subject to these changes.
Author Response
Comments and Suggestions for Authors Dear Authors,
Thank you for taking my comments seriously and greatly enhancing your manuscript. I no longer have any ethical concerns about the study.
In addition, your methodology and scoring system (and your reasons for using these) are now more transparent and your experiments would be reproducible.
The manuscript's English language has also been improved (although further improvements could still be made).
However, your discussion still significantly lacks discussion with regard to the literature.
- I suggest that you discuss your findings in light of some of the literature presented in your introduction.
Done: Line 449-463
- In addition, I recommend reading and referring to d'Ovidio et al. (2010)'Sex differences in human-directed social behaviour in pet rabbits'. Journal of Veterinary Behavior, 15, pp. 37-42 to discuss individual differences &
Added to the article to Methodology Line 188-195
Although according to d’Ovidio (et al.) online questionnaire (n=634) the chance of agressive behavior of the company pet rabbits against to their owner or a stranger person is significantly lower at intact males than neutered males and does and buck rabbits interest in their owner is significantly higher [d’Ovidio], the intact males spraying urine to determine their territory [Sharon]. We did not experienced the calmer temperament of the intact males and because of their urine spraying behavior we prefer using does for AAI works but by this examination we did not take into consideration the effect of gender to the AAI work.
- Mullan, S. M. and Main, D.C.J. 'Behaviour and personality of pet rabbits and their interactions with their owners.' The Veterinary Record, 160, pp. 516-520 &
Added to the article Line: 96-99
Rabbits struggle less if the owners frequently getting contact with their animals and confident in handling their rabbits. According to Mullan’s (et al.) observation rabbits with a regular companion spent significantly more time grazing, hopping and playing [Mullan, …..]
- Schepers et al. (2009) 'Welfare assessment in pet rabbits' Animal Welfare, 18, pp. 477-485
Added to the artice, LINE: 99-103
According to Schepers (et al.) findings the conditions in which pet rabbits are kept has a great effect on their welfare. Frequency of handling by the owner and the environment have impact on the behavior of rabbits: when solitary kept rabbits are being picked up they display strong resistance that indicating socialization problems and their lifespan is reduced […].
I also recommend some additional slight edits.
- Change 'imprinting' to 'socialisation' (or 'imprinted' to 'socialised' or 'imprint' to 'socialise') (as appropriate) in lines
15, done
21, done
22, done
129, done
- done
- Add further details about rabbit behaviour signals to your introduction.
For example, fearful rabbits can also crouch, have tense musculature, freeze, scan the environment/demonstrate vigilance, attempt to hide or escape, kick/struggle when held, scream, grunt, or thump.
Other signs of aggression include charging, biting, and raking with claws.
Some additional signs of calmness or relaxation include grooming, lying on the side or abdomen with hind limbs stretched out, and loose ears.
Inserted references:
Lines: 60-63, 81-84, 96-102, 103-106, 188-195
- Broom D.M., Fraser A.F. 2015. Domestic Animal behaviour and Welfare, 5th CABI Wallingford, UK, 462 pp.
- Forkman, B., Boissy, A., Meunier-Salaün, M.C., Canali, E., Jones, R.B., 2007. A critical review of fear tests used on cattle, pigs, sheep, poultry and horses. Physiol. Behav. 92, 340‑374.
- Mullan S.M., Main D.C.J. 2006. Survey of the husbandry, health and welfare of 102 pet rabbits. Veterinary Record 159, 103-109.
- Mullan, S. M. and Main, D.C.J. Behaviour and personality of pet rabbits and their interactions with their owners. The Veterinary Record, 160, pp. 516-520 DOI: 10.1136/vr.160.15.516.
- Crowell-Davis S.L. 2007. Behavior problems in pet rabbits. Journal of Exotic Pet Medicine 16, 38-44.
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- Please note that p= 0.02 was given in the caption for Figure 4 but not reported in the text.
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Overall, it is now clear that your research definitely has merit and should be published subject to these changes.
