Training a Giraffe (Giraffa camelopardalis reticulata) for Voluntary Foot Radiographs at Dubai Safari Park

Round 1

Reviewer 1 Report

This paper describes training a female giraffe to voluntarily participate in taking radiographs under behavioral restraint. Such information has been presented multiple times in professional symposia, but the training paradigm is under published in academic literature. As such, the manuscript would be of value to the academic and professional community.

 

That said, the manuscript requires significant revision. The work itself is no doubt remarkable and my comments and review are no reflection on their skill or ability to make this giraffe’s life more comfortable. I have concentrated my review on major aspects and examples of areas needed further clarification or revision as an aid to the authors in their revision, but therefore are not exhaustive.

Specifically, given the different terms used for similar objects or conditions (e.g., 'den' vs 'stall'), changes in writing style, and use of active voice in some but not all sections, I assume individual authors wrote different sections of this manuscript. I recommend rewriting or more extensive editing to ensure more consistent flow, tone, and terminology.

 

Introduction

 

Lns 35-36. Sentence as written is confusing between sex and species. Consider revising

 

Ln 38. "Operant based training" is not a common way of referring to operant conditioning or rewards-based training, which I believe the authors are referring to in this context. Suggest revision.

 

Ln 40. Suggest rewording - I assume the giraffe is naive to conditioning, and authors are not referring to a personality trait.

 

S 1.2 Housing. Lns 71-72 below refer to “breach in containment area” which should be described in this Section, or otherwise reworded.

 

S 1.2 Housing. What area did the training take place? What is the size of the pens? Description of the training space in Section 2.2 below is good, but recommend reference here to that information being further described below.

 

S 1.3 Diet. What was the frequency of feedings, specifically of the reinforcers, prior to and following being removed from display? What part of the day did the training sessions take place? Addressing questions like these will be helpful in other Sections when describing motivation and other setting events which influence training efficacy.

 

Ln 59. How was individual preference determined?

Methods

 

Ln. 102. Recommend using trainer or keeper, and not the two interchangeably.

 

Ln 102-103. Please further define "led the session" - we they observing and directing, involved directly in the training as the person who delivered cues, bridge, or both? Likewise with "oversaw the footwork"

 

Ln 104. Unsure what "mastered the behavior" means. Please clarify.

S 2.3 and S 2.4. Looks like sections 2.3 and 2.4 have the same title. Consider revising.

 

Lns 113-115. The second 'differential reinforcement' likely refers to stimulus discrimination, which may or may not include differential reinforcement. Consider revising.

 

lns119-123. Much of this information are common industry knowledge and can likely be summarized with citations.

 

Ln 124. Was continuous reinforcement only used during shaping, or in maintaining established behavior? Please define what schedules of reinforcement were used.

 

Lns 125-126. Please define what "the block" is

 

lns 129-132. Again, information can likely be summarized by citations

 

Lns 149-151. Are frequency and rate of reinforcements referring to the same condition of reinforcement schedule, or actual changes in the delivery of reinforcement to the giraffe? Please clarify

 

Ln 151. I would question whether "Hold" as trained in this manner is a unique behavior with an independent cue, vs duration built into the "Lift foot" behavior. The difference would be how the bridge was used, whether reinforcing for correct behavior but animal is expected to maintain current behavior, or if bridge was terminal and stopped the behaviors occurrence. As described here and previously, its unclear. Consider clarification.

 

Ln 151-190. I question whether this is an interdependent behavior, such as those above which were actively shaped by successive approximations, or truly active desensitization with the latter asking the animal to remain in position while additional stimuli are applied. For the latter, the animal is being reinforced for not eliciting any behavior other than "Hold" and "Lift foot", which are the behaviors under its control. I'd recommend "Front foot radiograph" not be included with the above shaped behaviors given the training techniques, as described, are different in application from the giraffe's perspective.

 

S 4. Radiograph positioning and Techniques. The style and condition of section is the most ready for publication in regards to succinct and clear presentation of information. Recommend the remainder of the paper be edited to fit this style.

 

Results

 

Ln 221. Please define “early morning’.

 

Ln 226-228. Were all primary trainers known to the animal? What other stimuli or events may have affected the animal's motivation? Better description of setting events may help readers understand motivation and behavioral attitude better.

 

Ln 229-232. Multiple references to the giraffe's ability to be distracted, her voluntary participation, and keepers providing patience have been made throughout the manuscript. I recommend a single section to focus on this in a succinct and clear manner, vs the current style which distracts the flow of the paper. 

 

S 5.2. Though true, this section is not necessary to the topic of the manuscript, and in itself is not a 'Result' of the training paradigm. I recommend removing it.

 

Discussion

 

The Discussion requires a rewrite, as much of the information included is new and does not directly relate to the topic of the manuscript. For a topic like this, I recommend the Discussion briefly reiterate the previous sections though further highlighting major and minor successes and flaws in the approach employed, and lastly identify alternative approaches that could have been used or could be in the future.

 

Author Response

Dear Reviewer,

Thank you for your suggestions, they were very helpful. 

I have attached a brief response to your points and will upload a revised version of the paper. 

Author Response File: Author Response.docx

Reviewer 2 Report

I like the paper very much. However, I would love to see the paper improved by few author's actions. 

- please include more precise description of the training, including the exact protocol of reinforcement schedule

- please include the training results broken down by days/trials

The exact, full description of the training and the results of the training will allow the readers to build his/her own comparisons and replications.

Author Response

Hello!

Thank you for your feedback, it was very helpful.

I have now revised the paper to include the exact protocol of reinforcement schedule.

I have now added a table in the results section, breaking down the training steps and sessions until the behaviour was mastered.

Reviewer 3 Report

Overall content was accurate and thorough. Just a few writing errors that I noticed:

Line51: "calm temperament of the this animal meant that they..."

Line 87: "reinforced and then targeted"

Line237: Desmond [5] (delete period)

Line358: "If (capital "I")"

Author Response

Noted on your feedback, errors have been corrected. Thank you! 

Reviewer 4 Report

Overall, this is a well thought-out manuscript documenting the basic training of a cooperative medical procedure. I like the way the author has focused on the cooperative aspect of the training and how programs like this can positively impact an animal’s life. There are a lot of run-on sentences and quite a few grammatical mistakes and spelling errors. Additionally, the author has a tendency to write as if speaking, specifically about what the giraffe “needed to do” throughout the training and procedure. Describing the procedure as giving the animal choice then listing all of the demands the animals needed to do gives mixed messages about your training program. You should rephrase those that sound like demands into something along the lines of ‘we waited for calm behavior before proceeding’ or ‘we always observed the giraffe and as long as she exhibited calm behavior, we continued’.

 

 

General comment: all scientific names should be italicized

General comment: in the abstract the scientific name of Reticulated giraffe is provided as two words, in the Introduction, it is provided with 3 words. When writing it out, please use the full scientific name consistently throughout the document. 

Overall General comment: all very tenses need to be consistent. Please choose past or present tense for consistency throughout the document.

Line 12: consider changing the first word ‘after’ to ‘when’ or ‘once’

Line 17: add a comma after ‘radiographs’

Line 26: First sentence is run-on, please rephrase

Line 26: add a comma after ‘popular’

Line 35: remove the word ‘currently’

Line 36: add a comma after ‘5 females’

Lines 45-47: This is a run-on sentence and needs consistence verb tense. Please add a period after the word ‘stalls’ in Line 45. Please choose past or present tense for consistency throughout the document.

Line 49: Please choose a consistent means of conveying plural numbers of animals; ‘hand feeding the giraffe’ and ‘each of the giraffes’

Line 51: please add an article such as ‘she’ or ‘it’ between the word ‘that’ and ‘often’

Line 58: replace semi-colon and word ‘this’ with a comma and the word ‘which’

Line 64: ‘retain their prey instincts’ sounds awkward. Consider rephrasing along the lines of ‘giraffes are known to defensively kick’

Line 72: change ‘escape options’ to ‘emergency egress’ (escape is almost always from the animal’s perspective, not the humans)

Line 78: after the words ‘secondary keeper’ change to ‘in close proximity of the hoof’

Line 82: change the word ‘as’ to ‘at’ and change ‘either side’ to ‘both sides’

Line 87: change the work ‘the’ to ‘then’

Line 87-89: This sentence is very awkward and run-on. Perhaps try ‘Training sessions were always voluntary. The giraffe chose to participate in all but two sessions.’

Line 100 & 112: These sections have the same heading. Choose a different heading or collapse these into one section.

Line 102: make tenses consistent (keepers/trainers or keeper/trainer) Or was it two keepers to one trainer? Please specify.

Line 104: animals master a behavior, trainers do not. Rephrase. ‘Once the primary trainer was confident the behavior was solid, it was passed on to other trainers.’

Line 105: the giraffe doesn’t need to display body language. I think what you mean is ‘The training session only proceeded if the giraffe displayed comfortable body language such as interest in training, relaxed ears and nostrils.’

Line 107: Change ‘dependant’ to ‘dependent’

Lines 107-109: If the giraffe was only trained for 15 minute sessions, how could you expect to maintain participation for 60 minutes during the radiograph sessions?

Line 114: What do you mean by differential reinforcement for teaching the gestural and vocal cues? If you mean you were teaching cues for the behavior this is an unnecessary statement. Cues are an intrinsic part of bringing a behavior under stimulus control and should not be described as a separate part of the process.

Lines 115-117: This is a runon sentence and needs consistent verb tenses. Consider ‘A systematic shaping plan was devised for each behavior. Each plan defined the goal behaviour, determined which approximations would be reinforced, evaluated the giraffe’s response and allowed us to revise the plan as necessary.’

Lines 119-120: Nicely stated

Line 124: You should stick with the phrase ‘goal behavior’ and not use ‘target behavior’ because you did, in fact, train the giraffe to touch a target. This is confusing.

Line 132: remove the words ‘that the giraffe knew well’ (high probability behaviors are self-explanatory)

Line 135: the giraffe did not need to maintain calm behavior, you only proceeded if she exhibited calm behavior. There is a difference.

Lines 138-140: If there was a set duration, please provide it. If the duration varied, please indicate that the animal was asked to hold until the clicker was sounded.

Lines 141-143: Separate these behaviors. I’m assuming the back up was to move backwards away from the trainer (not turn around and walk away), while the recall was to come towards the trainer but this needs to be explicitly stated.

Line 145: using the behavior in the definition of the behavior is circular and provides no definition. Describe what it looked like when the giraffe was at station. ‘The giraffe was considered to be at station (or stationing) when her chest was fully in contact with the straps, holding the strap in a horizontal position and leaning into the strap slightly.’

Lines 156-161: The whole paragraph needs restructuring. Perhaps, ‘Animal keepers desensitized the giraffe to a second keeper kneeling near the foot block but still semi-protected by the mesh gate barrier. Keepers slowly increased the duration the foot was on the block. Additionally the animal was desensitized to allowing keepers to move their hands in close proximity to the foot and eventually to touch the foot. Throughout this process, the animal was heavily reinforced for remaining calm and comfortable.”

General comment: Did you use just desensitization or did you also use counterconditioning? If you used food to actively reinforce the animal, you were counterconditioning. Desensitization is a passive process of acclimating an animal to a stimulus very slowly but does not generally involve food. Most positive reinforcement training programs use a combination of D/CC. Please be clear on these two procedures and which ones you used in which situation. (For example, leaving the food block in visual range during the session so the animal can see it is desensitization. Holding the foot block up, approaching it or interacting with it and using food to reinforce is Counterconditioning. Please look up definitions for these and use the appropriate terms.)

See:

Chance, P. (2013). Learning and behavior. Cengage Learning.

Domjan, M. P. (2014). The principles of learning and behavior. Cengage Learning.

McSweeney, F. K., & Murphy, E. S. (2014). The Wiley Blackwell handbook of operant and classical conditioning. John Wiley & Sons.

 

General comment: What does ‘calm and comfortable’ look like? What exactly are you reinforcing when the animal remains calm. Are you clicking for anything specific? Are you not clicking and instead are reinforcing with food every few seconds/minutes if the animal is relaxed? If so are you actually reinforcing relaxation? Chewing?  Please clarify what you were reinforcing here for this behavior.

Line 163: replace ‘of’ with ‘as’

Lines 167-171: This is a run-on sentence and is very confusing.

·        If touching the foot or being near it triggers a fight or flight response, it is NOT sub-threshold. It is over-threshold.

·        The word ‘parasympathetic’ is redundant when indicating a ‘fight or flight response’.

·        How is this a ‘fight or flight response’ if the animal did not walk away? If all the animal did was remove the foot but did not leave, then state that. To me, removal of the foot from the block does not indicate a fear response, unless there were other indicators of fear. It simply indicates the giraffe has not yet been desensitized to proximity and tactile behavior.

 

Perhaps what you are trying to say is that ‘Initially an object near the foot, or touches to the foot, caused the animal to withdraw the foot. After desensitization and counter-conditioning, the giraffe learned that allowing objects near the foot and touches to the foot were good predictors of food. This lead to a positive training experience and lack of fear response.’

 

Lines 177-183: This is a very long run-on sentence and should be 3 or 4 sentences.

·        Put a period after the words ‘radiograph equipment’ on line 179.

·        Put a period after the words ‘daily training sessions’ on line 180.

Line 181: verb tense. ‘Giraffes were’ or ‘Giraffe was’ (please clarify if it was one or many giraffes)

Line 182: the word ‘reinforces’ is not being used correctly. Do you mean ‘reinforcers’ or ‘reinforcement’?

 

General comment: presumably the animal was being offered food reinforcement throughout the desensitization process and not only when you were working to move the radiograph equipment closer to the foot. I’d move this sentence to the beginning of the methods section as a general statement that food was used to reinforce the animal during counter-conditioning.

 

Line 193: the words ‘the animal was weight bearing’ is conversational way to speak. Please change to ‘the animal was able to bear weight on its foot.’

Line 195: describe what a ‘head hike’ is. Anyone unfamiliar with giraffes will not understand what this is or what it indicates.

Lines 195-197: I would imagine a significant factor was also preventing the need for an immobilization of the animal?

Line 200: remove the word ‘that’

Line 202: change ‘effected’ to ‘affected’

Line 223: This is a run-on sentence. Please put a period after the word  ‘weekly’ on line 223.

Line 224: allowing to not participate is awkward. Perhaps ‘option of participating or leaving the session.’

Line 226: comma after the word ‘quickly’

Line 228: Please clarify- how was there variation in the skill level of one person? Did skill level vary across trainers?

Lines 229-232: Run-on sentence. Put a period after the words ‘training session’ on linke 231 and remove the word ‘however’

Line 237: Use commas between authors and remove the period after Desmond

Lines 239 to 242: when listing several items, use consistent very tense

·        Line 240: change ‘it affords’ to ‘by affording’

·        Line 240: change ‘expands’ to ‘by expanding’

·        Line 241: change ‘increases’ to ‘increasing’

Line 241: Do you mean ‘increases the quality of human-animal interactions’? Just increasing the interactions does not mean that they are positive. Please clarify.

Line 248: nice mention of CFL

Line 270: Please clarify which ‘issue’ to which you are referring. The issue of lameness? If the lameness was resolved, state that.

Line 288: Put a period after the words ‘valuable tool.’

Line 290: Put a period after the word ‘giraffe.’

Line 292: change the words ‘basic requisite’ to ‘important foundation’

Line 295: End the sentence after ‘at a target.’ Cut the rest of the sentence

Line 296-300: Run on sentence and very tense needs to be consistent. ‘Animal scan be trained to present body parts, and can be desensitized to objects and apparatus. This allows for examination and the use of non-invasive imaging techniques. Most importantly to the welfare of the animal, it allows for repeat treatments without the use of chemical or physical restraint, therefore minimizing stresss.’

Lines 304-306: of course animals in zoo have less control over their lives. That is one of the reasons why animal welfare is such a focus. Rephrase this sentence or remove it altogether.

Line 307: do you mean concept rather than precept?

Line 310: Is critical to what? Finish this sentence.

Line 312-314: This sentence needs work. Maybe ‘Training helps reduce stress as well as the risks associated with physical or chemical restraint.’

Lines 314-317: This sentence needs to be rephrased. Maybe “When training for potentially stressful medical activities (such as radiographs or blood draws), keepers seek a positive means of increasing the animal’s comfort with the behavior and all of the relevant stimuli, including people and equipment.

Line 321: end the sentence after ‘walking away.’

Line 322: what do you mean by ‘and an understanding’   Please clarify this phrase or remove it.

General comment: Is it giving the animal control that forms the bond and provides enrichment? I would argue that the bond is formed over time and with a history of reinforcement and trust. Control is important and can be reinforcing to an animal but is it itself enrichment?

 

For how control can be primary reinforcement, see:

Leotti, L. A., Iyengar, S. S., & Ochsner, K. N. (2010). Born to choose: The origins and value of the need for control. Trends in cognitive sciences, 14(10), 457-463.

 

Lines 331-336: Run on sentence.

·        Check the spacing of Line 332

 

Author Response

Thank you for your feedback and suggestions, they were very helpful.

I have now edited the manuscript.  

 

Author Response File: Author Response.docx

Round 2

Reviewer 1 Report

This manuscript remains an important addition to the literature on behavioral husbandry and applied behavior in zoos. I appreciate all the work the authors have done in the revision from its previous form. In its current state, the paper is much improved in consistency of terminology, style, and voice. Likewise, the Discussion section is much more in line with the manuscript overall, but I believe still requires edits. My other comments are below.

Lns 55-57: These sentences describing the individual receiving training seem more appropriate in Section 1.1 above

Ln 151: "the behavior was solid" is jargon; recommend, "...felt the behavior was trained reliably..." or "...felt the behavior was under stimulus control..."

Lns 155-156: Again, use of training jargon. Recommend, "...concentration level of the day and ended with a successful response or outcome." Since the 'jackpot' terminating the session was likely not part of the operant sequence, it either does not need to be mentioned or should otherwise be further described in operant terms.

Lns 159-160. Should include citations here

Lns 159-160: this paragraph is repetitive and likely unnecessary given the information presented in the paragraphs below

Ln 462: suggest "...allowed trainers to revise..."

Ln 259: suggest replacing "rewarded" with "reinforced" to maintain operant terminology; likewise, "highly rewarded/reinforced" suggests differential magnitude of reinforcement, which is likely not necessary for this manuscript so I recommend removing the word "highly".

Ln 267: correct the word "ytainer"

Table 1: this is an appreciated addition. Does the sessions column represent the total number of sessions, or sessions per behavior, i.e., multiple behaviors can be worked on within one session? Unclear, since for training to be completed within a period of 3 months with 4-5 session per week, that allots 48-52 sessions total. that is far less than the sessions described in the table, which is 176. Great information to have, but please clarify.

Ln 516: "capture her attention" is training jargon; recommend "redirected attention to the training session", or similar

Lns 522 and 528: again, replace "rewarded"

Lns 527-528: consider revising as 'agreement' among applied behaviorists is generally tested and statistically stated; consider focusing on the operant process in stating, "...it is important that all trainers maintain consistent criteria..." or similar

Lns 541-542: accurate, but I would recommend going further than stress alone to briefly highlight how training avoids the risks of anesthesia, especially in giraffe

Sn 6.32: Edit indent. Some of the information in this Section is a repetition of 6.2, and therefore not necessary.

Sn 6.3, 6.4, and 5.5: As with my previous review, I question whether these Sections are necessary as the manuscript is not evaluating the manifest aspects of training in agency, experience, or HAI. This manuscript adds to the literature on applied behavior and behavioral husbandry, which can be drawn on as an example of the efficacy of training and its affects on welfare, but I don’t think that discussion is needed or appropriate here. Given the length of the manuscript and its overall primary intent, I recommend authors remove these Sections.

Sn 6.6: This paragraph, similar to those above, has a different style and tone from the remainder of the manuscript. Recommend editing for consistency in voice, tone, and terminology (“hoof” in manuscript vs “foot” in this paragraph, protected contact vs restricted contact, "the animal" in manuscript" vs "the giraffe" in this paragraph, "goal behavior" vs target approximation", etc). Likewise, recommend editing for jargon vs operant terminology.

Lns 658-659: were the criteria relaxed (i.e., animal was reinforced for previous approximations within the current session) or was training paused to be evaluated for safety? Please clarify.

Ln 659: this sentence states the session would be ended early with onset of signs for uncomfortably or agonism, however previously the sessions "always end on a positive note". Please revise for consistency.

Author Response

Thank you for your feedback

Author Response File: Author Response.docx

Reviewer 2 Report

Although I would prefer more detailed protocols of training, I am ready to accept the paper in its present form. 

Author Response

Thank you for your feedback

Reviewer 4 Report

Comments for author File: Comments.docx

Author Response

Hi, thank you for your feedback.

I have made the recommended revisions, although we seem to have a discrepancy in line numbers.  

Author Response File: Author Response.docx