In Absentia—Can a Lack of Behaviour Be a Useful Welfare Indicator? An Application to the Captive Management of Livingstone’s Fruit Bats, Pteropus livingstonii

Round 1

Reviewer 1 Report

Comments and Suggestions for Authors

 

Introduction:

In general, the introduction is clear and easy to understand. However, some transitions, between two phrases, are too abrupt. Furthermore, in the way is redacted, absence of locomotion is seen as an absence of behaviour, which I don’t fully agree, since it is not an all or nothing behaviour but rather a quantifiable (time spent) one with two extremes fully active and fully sedentary. Non the less, this is only “semantics”, and the idea authors want to transmit is easy to understand.

 

Lines 69-71: Why give them supplements then? Why not adopt a better diet?

 

Lines 78-85: How long do they live in the wild?

 

Materials and Methods:

This section is easy to read however, I had some questions and issues.

 

Lines 172-173: You said more or less the same earlier (lines 120).

Lines 177-179: How many veterinary checks were done over the studied periods? Did the body mass was measured before and/or after an observational period (‘summer 2019’ and ‘spring 2020’)?

Lines 202-203: So why mention it?

 

Table 1:

                  Why explain by sub-category, when they didn't use in the analysis?

                  In the sub-category forage, the animals are stationary?

                 

Lines 212-216: This passage is difficult to understand, when you mention “sampling time” and “samples”, is data from one individual or all the individuals. As I reeded, this part “The proportion of the sampling time during which the focal individual carried out a behaviour within this category was then calculated” is for one individual, and “On examination of these data, zero-inflation was apparent as there were a large number of samples when the focal individual did not carry out one of these behaviours (81.5% of samples did not include foraging behaviour, 48.8% did not include locomotion, 39.7% did not include vigilance and 31.6% did not include roosting)” is for all the individuals. Which is a bit confusing.

 

Lines 229-234: I am not at all an expert on statistical analysis, however I am not quite convinced that age should be excluded. Firstly, why not use age instead, since it is more easily known? Secondly, since you are trying to predict health issues, accounting for variance might improve the accuracy of the model.

 

Results:

In general, is the number of observations per individuals more or less the same? How come the identity is not considered in the models?

 

Lines 253-255: When where diagnose these 11 individuals?

Lines 255-257: Is this normal for wild bats? Or it is a consequence of captivity.

Lines257-259: It is not clear if the total time is on each individual or for the overall observations.

Table 2: What does the asterisk mean? There is a tabulation problem in the last line of the table.

 

Figure 1:

Did you use a discrete measurement for body mass, if yes why?

There seems to be bimodal or trimodal distribution. 

How many of these points are the same individual?

Legend: You mention the black line and the shaded area but not the black points.

 

Figure 2-3:

                  Legend: Please mention the number of individuals in each category.

 

Lines 277-278: In figure 4, how is this regression made, is it weighted, and did you check for normality? Because, the proportion of not foraging of the smaller and larger body mass, is within the variability of the intermediate values (between 700 g and 1000 g), which are the most frequent ones. Moreover, for intermediate values of body mass, where most of the samples are, the variability of not foraging behaviour is the largest, how do you explain this?

 

Figures 1 and 4: Why do you show the many data points per individual (figure 1) and then only one per individual (figure 4)?

 

Discussion

 

Although not the main objective of this work. I think that a small comparison, in the

Discussion sections, between wild and captive animals might improve “the attractiveness” of this work, mainly could these non-invasive methods be used on non-captive animals?

 

Did you account for rhythmic or asynchronization activities? Which may or not depend on dominating, non-dominant male are more likely to be less active during some hours of the day or when dominant are active (or vigilant). You answer more or less this in the discussion (lines 386-389), but not for your data.

 

 

 

 

 

Author Response

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Author Response File: Author Response.docx

Reviewer 2 Report

Comments and Suggestions for Authors

Interesting examination of an alternate method of using behavior as a welfare monitoring tool. The reasoning in the intro and discussion is sensical. I was a little confused as to the data collection and presentation and had questions as listed below:

 

Line 32. “More traditional methods…” Traditional methods of what? Husbandry or assessment?

Line 36. Change state to “states” to much plural animals

Line 37. Remove “a” before captive environment, change environment to “environments” to match plural

Line 44. Add comma after habitat “destruction”

Line 67. “this means…” This what? “This” should always be followed with a subject. Possibly “limitation”?

Line 94-96. “is therefore too late to effectively treat…” This line is confusing—presumably you mean the symptoms arise after disease progression is such that it can’t be treated. Maybe change to “disease has progressed too far to effectively treat…”

Methods: In general, I think this section needs more detail. For one thing, I missed at first read that apparently the observer is actually in the bat habitat during observations?

Line 139-140. How many of these bats were the same between seasons? What was age range of males?

Line 144. Assuming tags were installed prior to study. How far from the subject could the tags be read? Where on the bat were they installed? Was it frequently necessary to use the RFID to make identification?

Line 181-182. These observations were performed live using tablet? No video recording? Do the 5-6 hours of observation represent a single long session or shorter sessions throughout day?

Line 182. For all random orders you mention, how were they randomized? Using an app or website, etc?

Line 182. Was there any attempt to balance random orders—that is, so that approximately every day of week was observed roughly evenly to account for differences in attendance (for example, in case weekends had more guests), husbandry differences due to day, etc.

Line 185. I’m having trouble visualizing these 42 sections, especially since later parts of the publication suggest that the observer was also in the habitat. If viewed from above, are these rhomboid sections arranged in a grid? Can you supply a map to show these sections? Do they stretch floor to ceiling?

Line 192. This… Add “method,” for “This method…”

Line 194. A little confusing, since individuals could be moving in and out of sections. Did observer note which individuals were in section at start of observations, or did observer just randomly choose a subject to start with and moved on to the next random subject present in the section once prior subject’s observations were complete? Or if subject changed sections, did observer continue observations from the section the prior subject ended in?

Line 198. Again, some confusion about observations and subject. During each day, was each subject observed? If so, that’s 20 or 22 subjects for 10 min, 22 x 10 = 220 min, or 3.7 hours. Where does the 5 to 6 hours (line 181-182) come from? Locating and switching subjects between focal periods?

Line 229. Did the relationship between age and weight always increase, or did it eventually level off? That is, were always older males always heavier? Was there any kind of geriatric effect for very aged males near end of life?

Line 245. Again, does this ethics section confirm that the observer is in with the bats? If so, that info should be introduced earlier.

Line 263, Table 2. Maybe I missed something obvious, but why are some of the entries just *?

Line 273. I might not have expected an effect for season in a controlled interior environment—interesting that you found one!

Line 318-319: Could smaller or younger individuals require less food and result in less foraging?

Line 339. You explained well your model selection process, but I wonder how different the results looked with age instead of weight as a factor? A lot of these behavioral differences you mention could have age-related causes.

Line 351-352. Interesting that the results suggests that dominant individuals don’t watch for challengers.

Line 363. Was there any relationship between foraging and vigilance behaviors?

Line 388-389. Thanks for bringing up the after-hours behaviors of captive animals, especially nocturnal ones. Always good to keep in mind.

Line 391. A final thought: How time consuming would you say looking for absences of behavior would compare to looking for specific worrying behaviors? Granted, not all instances of poor welfare are expressed through behavior (hence the purpose of the study), but I wonder if it is harder and more time consuming to observe and quantify the absence of a behavior, since it first requires determination of an activity budget, which can be time consuming for animal care units that are short staffed or just simply lack time for observations. It seems the observations in the project were carried out live and took 5-6 hours daily—that’s time no keeper team can be expected to devote to just observation. Do you have any thoughts about recording behavior via video? What about using some tech solutions to determine when a behavior seems absent? What about minimum required time or method to detect the absence—that is, maybe even just 1-0 sampling instead of continuous? We have to consider time spent needed to use your methodology to ensure that looking for absences is a good use of time.

Author Response

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Author Response File: Author Response.docx

Reviewer 3 Report

Comments and Suggestions for Authors

The manuscript describes a study of potential behavioural indicators of compromised health in the critically endangered Livingstone’s fruit bat in captivity. Given the rarity of the species and the necessity for their ex situ conservation, this paper fills an important gap in the knowledge of the health management of this species in captivity. As presented, the manuscript is not yet ready for publication but has the potential to be an important addition to the existing literature.

At a conceptual level, the paper does not provide a new perspective. The idea of using both the expression or lack of expression of specific behaviours as welfare indicators is not novel and has been part of the theory of animal welfare assessment for some time. However, quantifying this effect is important and it can offer new insights into aspects of welfare which would otherwise be overlooked.

As it stands there are two problems with the study. The first relates to the aim of the study in relation to the methodology. The stated aim is to identify behavioural indicators associated with obesity and other health problems in captivity. With this in mind, exactly what constitutes obesity is never defined, nor are the other health problems that are apparently the focus of this study ever described. Assuming that some standard diagnosis was used to classify the animals as obese, the sample should be drawn from obese animals specifically – this appears not to be the case. Thus, from the perspective of the reader, the authors attempted to investigate obesity (which has no clear definition in this context) in a population which, as far as the reader is concerned, may or may not include obese individuals. There is incongruence between the stated aim of the study and how the data collection is approached. This needs to be addressed, either through providing the reader with far more information about the subjects of the study and the methodology or by reframing the aim of the study in terms of obesity risk rather than obesity as an outcome.

The second issue relates to the methodology employed in the analysis of the data and the reporting of the results. The variables under consideration are behaviours which as treated as independent outcome variables. However, by their nature, the behaviours cannot be considered independent because they are mutually exclusive. Feedback is provided in the specific comments but the analysis does not seem to be appropriate, given what is being analysed. Further to this, the analysis would potentially need to be modified according to whatever changes are made to the study aims. The results presented are incomplete. There are missing contrasts in the model outcomes and these are very apparent. Without these, the reported results only provide part of a picture of what was examined and limit the applicability of the findings.

There are other, smaller, issues with the manuscript which the authors will need to address. With this in mind, the manuscript has the potential to be published should these issues be resolved. As a result, I am recommending that the manuscript undergo major revision prior to resubmission.

Comments for author File: Comments.pdf

Author Response

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Round 2

Reviewer 3 Report

Comments and Suggestions for Authors

Thank you for your response to the feedback provided. The manuscript is improved following the changes that the authors have made. There are two minor issues that need to still be addressed though, as listed below.

1) The phrasing of the aim is the reverse of the statistical methods employed. The aim states that the study seeks to identify behavioural indicators of increased body mass and other health issues. Thus, the appropriate statistical design would be to use behaviours as predictors of body mass and other health concerns, whether through modelling or simpler correlational approaches. However the statistical design employed does the opposite - using body mass and other health concerns as predictors of behavioural expression. The wording of the aim should be amended to better reflect the method being used. It is a minor point but technically the aim and methods should align.

2) Page 4, Lines 175-176: It is not clear if the body mass data referred to here was gathered per sample period or once-off at the end of all the sampling. If the latter, this is problematic because it would mean that the behaviour records are decoupled from the body mass measures that are being used in the modelling. If the former, this should be stated clearly.

With these minor issues addressed, I see no reason why the manuscript will not be ready for publication in Animals.

Author Response

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