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Peer-Review Record

Seasonal and Daily Activity of Two Zoo-Housed Grizzly Bears (Ursus arctos horribilis)

J. Zool. Bot. Gard. 2020, 1(1), 1-12;
Reviewer 1: Anonymous
Reviewer 2: Anonymous
Reviewer 3: Anonymous
J. Zool. Bot. Gard. 2020, 1(1), 1-12;
Received: 23 July 2020 / Revised: 20 August 2020 / Accepted: 21 August 2020 / Published: 25 August 2020
(This article belongs to the Special Issue Recent Advances in the Science of Zoo and Aquarium Animal Welfare)

Round 1

Reviewer 1 Report

The aim of the study was to observe two grizzly bears in captivity for over a year and study their seasonal and daily activity. The researchers collected 451 hours of behavioural observations, which is remarkable for zoo research. I have some general questions and comments to improve this paper and some specific remarks. Overall, I think that this paper might be interesting for publication in the Journal of Zoological and Botanical Gardens. However, some adjustments need to be made and the discussion should be improved.

General questions and comments of improvement:

The introduction is based basically in brown bears (in general) but the study is in grizzly bears. Perhaps it could be more centred in grizzlies?

Materials and Methods: did the bears have any other type of environmental enrichment besides food-related enrichment? Which amount/%/proportion of the diet was used for the environmental enrichment?

Statistical analyses: why was the decision of combining January months and July made? Why were the rest of the month excluded from the analysis?

Figures 1, 2, 3: add the full name of the behaviours on the legend: Stereotypic or Stereotypies, Inactive. Also, there is sometimes a spelling mistake of the word Active (it says Acive). In the footnote of Figure 3 I would add that there were extra observations done in July between 16 and 18h to explain the extra data on the right side of the bottom graph.

Discussion: from the references cited, food availability seems important for the level of activity of the bears in the wild, but it should be discussed better how this information affects your study. It is confusing how you relate this information to your data, especially because you mention a reference that says ‘both the daily and seasonal activity of brown bears is likely most sensitive to food availability, as opposed to daylength or temperature’. However, in zoos the availability of food is usually controlled. How would you discuss that the seasonal activity is most sensitive to food availability in a controlled environment such a zoo?

I think the discussion should be improved. I am not sure that it benefits from the subsections. Maybe clearer paragraphs without subsections would be better and make it easier to read. For example, the information related to stereotypies is described in 4.3 Daily Activity, when I believe it would fit better in subsection 4.2 Stereotypies. There is a lack of information related to anticipatory behaviour, which seems a trigger for the repetitive behaviours that the bears showed according to the descriptions from the authors.

Conclusion: all the text in the conclusion is more for the introduction or the discussion, but not for the conclusion. The conclusion, if you want to add it, should include a summary of the findings of your study.

More detailed comments follow:

L27: ‘inhabiting a variety of habitats’ sounds too vague, is there a range of habitats that could be added as examples?

L58-64: I would add here some of the difficulties to use stereotypies as welfare indicators: they can also be a reflection of previous/past problems, not just from current siatuations.

L65: add a small summary of the conclusions from the studies referenced (references number 44-46).

L80-82: the writing is confusing. Maybe something like this would be clearer for the reader: ‘Two captive-born grizzly bears (Ursus arctos horribilis) were the subjects of the study: Keema, a 15-year-old, ~395 kg male bear, and Denali, a 15-year-old, ~405 kg male bear. Both animals came from Washington…’.

L81: ‘at the start of the study’ is extra information added for just one of the bears. This is confusing, as it rises some questions: were there differences before and after the study? Were they important? What about the other bear? I would delete these words unless there is important to notice that there was a big difference in weight before and after the study; in which case should be specified.

L87: lowercase after colon: ‘an on-view’, instead of ‘An on-view’.

L108: does this program have a specific name?

Table 1: there is an extra space at the beginning of the word ‘Standing’ (L127). Could the definition of ‘Pacing’ start with another word (maybe ‘walking’?), so the word that needs to be defined it is not used as the main word on the definition?

L172: ‘made the ethogram exhaustive’. Not really, since you might be missing other behaviours that might not be important for the study, but that does not make the ethogram exhaustive. Maybe better to delete this part.

L174: 30 min instead of .5 hours.

L177: how many observations per day were on average? Were they scheduled? How did you choose which specific hours to observe every day?

L210-211: maybe it flows better if it reads something like: ‘except for three months: 19.9%  in May (SE = 1.8), 18.4% in June (SE = 2.7), and 17% in July (SE = 2.6).’

L222: it should be ‘Between January and July’ instead of ‘From January to July’.

L274: 17-20% of stereotypic activity is not low…

L290: by saying ‘comparing the months of January to July’ one understands that the comparison was made among all months from January to July (so 7 months in total), while for what I understood from the study these two months were compared one (July) to the others (two January months). Maybe ‘comparing the months of January and July’ is more accurate?

L292-295: it sounds that the animals are showing anticipatory behaviour to feeding times. It should be better described and referenced.

Author Response

See attached file.

Author Response File: Author Response.pdf

Reviewer 2 Report

Major comments

This is an interesting study, and I am especially intrigued by the potential explanation for the timing of the stereotypical behavior in bears, which coincides with the mating season. However, I also do see potential for improvement of the paper, especially in relation to the methods used. The paper strikes as not quite appropriately analyzed; also, several important methodological details and justifications are missing. Below are some comemnts that I hope will help the authors imporve their manuscript.

Minor comments

  1. Title: Ursus arctos horribilis, arctos and horribilis should not be in capital letters
  2. Lines 31-33: Based on more recent data/papers and technology, bears do not increase their activity before denning, rather the time period before denning shows comparatively low activity. See for example, Evans et al. 2016. Drivers of hibernation in the brown bear. Frontiers in Zoology 13. This would in general be a very useful citation for the authors to use, as it shows the temporal activity patterns of wild bears brown bears in the course of a year.
  3. Line 62: delete additional space between are and attributed
  4. Line 74-75: based on focus a), I expected to see actual comparisons with data from wild bears. As no such data are presented, the authors might want to done down this sentence a bit.
  5. Line 82: Delete scientific name, double
  6. Line 98: Diets varied…seems like a word is missing.
  7. Line 111: “the” Dr. James C. Ha?
  8. Line 120: Just wondering how the ethogram was developed? Are there some citations to support this?
  9. Table 1: It seems like the format of Table 1 was destroyed either during the uploading of the manuscript to the journal, or when I downloaded and opened it. Due to this error Table 1 is really difficult to read and understand, at least in my version of the manuscript.
  10. Line 175: typo – portion
  11. Line 175: how were observations spaced throughout the day? Randomly, evenly distributed, were sufficient numbers of observations taken during each time period during the opening hours? How many different people observed the bears? I doubt that it was one of the authors, as the data is rather old. Did all observers obtain training, etc.
  12. Lines 179-186, Statistical analysis: based on the introduction and the statistical methods described in this paragraph, I have a hard time understanding how the authors analyzed their research questions 1 and 2. Changes in hour to hour and month to month activities seem best suited for linear or non-linear models. Based on this paragraph, I do not understand what exactly is compared with MWU tests – linear patterns cannot be compared with MWU’s.
  13. Line 182: I suppose the n is the number of times a given behavior has been observed? And then the numbers were than analysed as proportions. This information should be mentioned in the statistical methods.
  14. Line 190 and more: is M referring to the mean? I am more used to seeing x-bar or spelling out “mean”. I also noticed that the authors report SE, and not SD. The authors should use SD if their intent is to describe the variation of a measurement and SE if they want to report the uncertainty around the estimate of the mean. It is my understanding that the authors are more interested a description of the variation around the mean. In addition, the SD is usually not affected by the sample size, while SE usually decreases with an increasing sample size.

Given that the authors state they are working with MWU tests in their methods, the authors should also report the median and the range of all measurements and especially in their results, as the MWU is non-parametric and uses median and not the mean.

  1. Line 197: Figure texts should be stand-alone. Or is this a one-sentence paragraph – if so, please attach to previous paragraph.
  2. Legend Figure 1: Type: Acive, instead of active!
  3. The data are not analyzed to their full potential. GAMMs could have been used to show if there are temporal trends in behavior over time.
  4. I was surprised to see this much activity and especially feeding in January. It seems like these bears were not really kept under very natural conditions, are during this time of the year, brown bears at these latitudes should be hibernating. This suggests that the behavior of these bears may not be very natural, which again makes it very difficult to compare to natural behavioral patterns of wild bears.
  5. 203-204: How are the winter months defined?
  6. Line 212: It is unclear for a reader why the months January and July are compared. This comes a surprise and is not described or justified in the introduction or the methods. With the use of different statistical methods (liner or non-linear modelling) all months could have been compared. At least it would have made sense to divide the year into 3 seasons based on bear biology (hibernation, mating season, hyperphagia) and compare the differences between these seasons.
  7. Line 220: given that the authors used MWU tests, they probably should use median and range rather than mean and SE, as a MWU test compares medians, and not means.
  8. Lines 233-244 and Figure 3. Also here, why not use linear models to compare? The descriptions of the activity curves are only verbal, no measures of significance are given. This could be easily done with non-linear models, or at least with Anovas.
  9. Legend Figure 3: typos: acive and inacti
  10. Line 250-252: it seems like these zoo bears were fed through the entire winter, and were also on display during winter. This is very different behavioral and feeding rhythm compared to wild bears. The decrease in activity is similar, but wild bears basically go to zero food and total inactivity while the bears in this study “only” decreased the other activities. This may hamper a comparison with wild bears.
  11. Line 253-256: it seems like your bears were actively “herded” into the display area, in other words, they had no other choice but being active! This may not be what they actually wanted to do. I am wondering how much of your behaviors are caused by the bears being forced on display rather than by choice of the bears themselves
  12. Lines 258-262: this is a difficult comparison. True, brown and polar bears are closely related, but polar bears do not hibernate during the winter months, while brown bears do. I am therefore struggling with this behavior comparison during the winter months.
  13. Line 268-270: This is an interesting statement, but this is likely not the case in bears, as especially male bears forage very little during the spring months, which coincides with the mating season.
  14. Could stereotypical behavior have been affected by the amount of visitors? In general, could the behavior of bears be affected by the number of visitors and temporal visitation patterns?

Author Response

See attached file.

Author Response File: Author Response.pdf

Reviewer 3 Report

TITLE: correct “Horribillis” to “Horribilis”; suggestion: Seasonal and Daily Activity Patterns of Two Captive Grizzly Bears (Ursus Arctos Horribilis)

Lines 24-25: Consider „behavior“ instead “behavioral observation”; delete “daily activity”, “grizzly bears”, “seasonal activity” and “Ursus arctos”, they are all in the title

Line 27: consider replacing “Wild” with “Free-living”

Lines 35-36: replace “the methods include” with “these methods included”; for radio collar tracking include all references that used radio tracking, e.g. no. 2, etc; consider to replace the whole sentence with “These methods included mostly radio collar tracking, scat interpretation or a combination of one or more methods. Contrastingly, in captive environments direct observations and human interference are plausible.”

Line 80: delete “Ursus arctos Horribilis”

Line 90: move sentence “Devices such as boomer balls and feeding enrichment were regularly placed in both areas.” in line 100 after “…depending on availability.” and add word “outdoor” in between “both” and “areas”

Lines 93-96: join sentence “The bears were typically moved from the off-view area to the on-view area by 0900 h, and then limited to the on-view area of the exhibit between 0900 and 1600 h (Fall/Winter; October – March) or 0900 and 1800 h (Spring/Summer; April – September), with some variability depending on the season and weather.” to previous paragraph

Line 96: delete “season”, add “conditions” after “weather” because seasons are already defined and just according to different weather conditions bears would be moved

Line 96: start new paragraph about bear diet

Line 105: add in Subjects and Setting a sentence explaining that even though bears had a denning area at the Zoo they did not go into hibernation and they were fed regularly on daily basis (2 times per day if I understood correctly)

Line 127: delete space in front of “Standing”

Lines 194-196: delete “For the purpose of analyses, only the classes of behavior that occurred more than 5% (i.e., Inactive, Active, Forage, and Stereotypy) were examined for month-to-month and hour-to-hour activity, as well as statistical analyses.” and move a part “Only the classes of behavior that occurred more than 5% were examined for month-to-month and hour-to-hour activity, as well as statistically analysed.” to line 182 after “…statistical analyses.”

Line 198: stitch the sentence to the remaining text (lines 191-193) without making a new paragraph

In the legend of Figure 1 correct “Acive” to “Active”

Line 205: “frequencies” instead “frequency”

Line 212: describe shortly (1-2 sentences) why the comparison is between January and July, why not August. And stitch the sentence “Figure 2 shows …” to the same paragraph

Line 227: move the sentence at the end of paragraph about hour-to-hour observations (line 245)

Line 228: move Figure 3 after the paragraph about hour-to-hour observations (line 245)

In the legend of Figure 3 correct “Acive” to “Active” and “Inacti” to “Inactive”, delete spaces in front of “Forage” and “Inactive”

Line 234: replace “In the January months” with “In January”        

Line 242: correct “decease” to “decrease”

Line 250: add “(hibernation period)” after “… being inactive”

Line 251: replace “as discussed” with “as mentioned”

Line 263: add 1-sentence about food availability and activity during hibernation period in free-living brown bears; reference: KROFEL M, M ŠPACAPAN AND K JERINA. 2016. Winter sleep with room service: denning behaviour of brown bears with access to anthropogenic food. Journal of Zoology 302:1–7.

Line 265: Move 4.2 Stereotypies after 4.3 Daily Activity, i.e. Daily Activity goes after Seasonal Activity and become 4.2

Lines 311-312: put first „seasonal“ then „daily“

Author Response

See attached file.

Author Response File: Author Response.pdf

Round 2

Reviewer 2 Report

Thank you for the reply from the authors. I personally still feel that the authors under-utilize their data by just comparing January and July with MWU-tests. If the sample sizes are too low for more advanced analyses, then the authors should at least point out the absolute number of behaviors collected, and not only frequencies. It seems like 140 sessions were carried out in January and July, which should have resulted in a decent number of behavioral observations. However, with only frequencies presented it is difficult for a reader to judge overall sample size and if Anova’s would be possible. Also, their justification provided for choosing January and July is not convincing. The fact that these periods are 6 months apart does not reflect bear biology, and the second argument that these are common months for such comparisons are not based on any biological or ecological argument at all. I suggest that the authors rather should argue that January reflects the hibernation period and July the mating period; this would reflect a biological argument and also would support their interpretation of the data. In general, a bear’s year can be divided into three parts: hibernation, mating season, hyperphagia season. The authors could have even compared these three seasons based on bear biology.

Author Response

We have included a seasonal comparison that utilizes Kruskal-Wallis ANOVA on ranks tests. This information is presented via a graph (Figure 4), as well as described in terms of the ANOVA scores and the means and SEs of those seasonal differences. The manuscript has been updated to reflect this change.

By adding this seasonal comparison, it sets up the following January verse July comparison. We address this comparison now in two places (Methods and Results) as such:

Methods (end of Statistical Analyses): "January and July were directly compared because they were representative months for further examinations of the seasonal differences between the traditional winter (January) hibernation and summer (July) activity periods."

Results (after seasonal comparison): "To further examine the behavioral differences that occurred seasonally, we compared two months (January and July), which in the wild would be representative of winter hibernation and summer activity periods, respectively."

Also, aside from editing the entire document to reflect these changes, we added a couple of pictures of the bears in their exhibit. These should help the reader see examples of two of the behaviors (Lying Down [Inactive] and Standing [Active]) as well as give clear visuals of what their on-view outdoor portion of the exhibit looks like.

Round 3

Reviewer 2 Report

No further comments

Author Response

Thank you for your valuable input.

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