Influences of Rearing Environment on Behaviour and Welfare of Captive Chilean Flamingos: A Case Study on Foster-Reared and Parent-Reared Birds
Round 1
Reviewer 1 Report
I would first like to state that this is perhaps one of the most thorough sets of data that I have experienced in a paper in my 30 years of science. Very impressive!!!
After reading through the entire paper, here is my overall gestalt: The two species of flamingoes are really quite similar, and while the minimal differences between the two are well explained, the authors really state that the big difference is their phenotype/appearance (lines 117-19). Indeed, other potential differences, in my opinion, are also probably lessened given the pretty similar rearing conditions between the two groups, as opposed to had these been reared and then transferred to very different places. So, the control and experimental groups are very similar, really. Thus, after all is said and done, after the massive analysis, I am really not surprised that no major differences between foster and parent reared chicks were observed.
This lack of difference would have been more satisfying if there were data that were out there suggesting that this experimental set up might be really important, given a significant negative trend that has been observed. Indeed, there appears to be no literature, beyond the fact that Chilean flamingoes are more endangered, and this important to determine if a broader suite of husbandry practices could be useful, to suggest that husbandry, in general, of Chilean flamingoes is problematic. There are not references on success rates in other studies, if survival of Chilean flamingoes in captivity vary from other species, etc. I guess I am saying that a better set up of the conservational importance of this study would be warranted. It is a very very very complete analysis of behavior results of the two systems…but if the reason we do this is just because we happened to have this accidental cross-fostering event at the facility, is less compelling. If you make me more interested in why this might be of some pretty important conservational concern, then, at the end, I’ll be very happy that it seems like this example of an alternate rearing paradigm seems to be ok, and thus potentially beneficial for the conservation of this endangered species.
Now I will return to the paper and work through some points as I move through it:
Introduction:
This paper is ultimately about parent rearing vs. cross-fostering of the Chilean flamingoes. The introduction got me a bit lost in the weeds, adding hand rearing, foster rearing, and peer-rearing, to the mix. There must be 100% clarity in the differences. Perhaps a better table defining what I think are the 5 possibilities that are variously brought up/discussed in the introduction...such as:
Parent reared – by mom and dad (which was done here)
Hand reared – by a human
Peer- reared – by same species with other chicks in brood
Fostered- reared = by same species with no other chicks in brood
Cross-fostered by DIFFERENT species (no idea about other chicks around??) also done here, correct?
Indeed, I think the definitions above are correct, but peer-reared, in particular is a bit confusing to me…. Is foster-rearing only reared by a same-species parent with no other chicks? Is peer-reared only same species? Is there a difference when you are cross-reared if your foster parents have other chicks or do cross-foster-parents never have chicks of their own species? These are the questions that came to mind as the authors worked through past studies of these different systems.
With a better definition/distinction of the different rearing types above, ultimately, perhaps some of my confusion in the introduction would be reduced, if terms are stuck to, and references are appropriately classified based on what types of rearing systems were studied.
Here is a specific example of my confusion: Paragraph starting on Line 74 “Indications that the early…..”, the numerous examples from the first part of the paragraph (sandhill cranes, moles, deer, etc.) all refer to cross-fostering studies (parents NOT of the same species). However, the final example of the Nene study (reference 44) appears to be a foster-rearing type study – with only Nene involved (granted, in different types of interaction between parents and chicks). Thus, the background comparison/set up for the experiment here (which is really a study of cross-fostering vs parent-reared study).
At the end of the day, the introduction would either benefit from a reduction to focus on parent- vs cross-fostering background studies alone, or a significant re-write to make sure the various other methods are defined well, and background studies compared consistently. I see how the latter can be frustrating, as I imagine the literature is a big mish-mash of comparisons between multiple rearing methodologies.
Lines 97-101: You say “authors have advised against, and limited, the use of fostering as a husbandry technique for reintroduction programs…”. Cross fostered? Regular fostered? Fostering in general? Is this a statement that unless you’re raised by your own mom and dad, it’s a problem?
Paragraph starting line 106: HERE is the place where it would be nice to have further discussion of the importance of this comparison beyond the ease in designing the study. I might even perhaps leave off or modify the sentence starting “Behavioral differences…” as you are basically saying that, since these two are so similar, we probably aren’t going to find differences……
Methods:
I apologize if I missed some of these details.
- Are the two species kept separate in the exhibit? Flocks of Chilean and Andean flamingoes do NOT interact directly? This is important to establish….once the foster chicks are moved back, they have no chance to see their foster parent. This was not obviously stated. (See line 153 – describing where the Chilean flamingoes reside, but no mention of the Andean)
- Observations: I’m confused between the scan sampling data and the photographic data. How did the two methods contribute to the variables measured? Were the behaviors from the ethogram determined from photos? From live watcher? This is unclear.
- Statistical analyses: I have no competency to evaluate the appropriateness and or correctness of the statistical tools used in these analyses. I will assume that they are the correct methods to use to make these comparisons, and the statistical comparisons/tests used to compare the two groups of chicks is appropriate.
Results:
As stated above, I must say that this is a pretty impressive (perhaps daunting might be a more appropriate word) set of results. The details are Greek to me, and I wonder if the massive tables might be more appropriate as appendices or supplementary information, if those structures are available in the JZBG.
Overall, the ability to glean results from a subset of the figures (#3, 4, 5 & 6) is 100% dependent on being able to see the paper in color. I, personally, prefer to still read papers on paper, and initially printed this in Black and White, which made it impossible for me to follow results well. This is perhaps not a fault of the author, but perhaps a concern for the Journal as a whole.
Figures 3, 4b & 5: a better distinguishing line between the months would be helpful. (between the PAM and SHB of each month). Additionally, it is interesting that the foster chicks are all represented individually (and no comparison/distinguishing of sex of the 6 of them) and then compared to the groups of female and male parent-reared chicks. Would a summary bar of the 6 foster chicks, compared then to the parent-reared chicks be more informative? Would you see any differences more readily? I often find pause when individual data (i.e., the 6 foster chicks) are put out, when it is the GROUP data that we are concerned about. I guess my point is that, beyond the differences in how the different behaviors vary from top to bottom, the comparisons between groups of birds is less compelling.
Figure 4: If color is the go-to here, note that the description of colors in the caption of figure 4A (gray scale) are not consistent with the GREEN scale in the color figure.
DISCUSSION:
Might the discussion begin with a version of the paragraph starting at 634. I think it would be nice to know at the start of the discussion that there appears to be no major issues between Chilean flamingo chicks reared by Andean parents or their own Chilean parents.
Then, perhaps, the more detailed differences can be discussed.
Grammar issue line 610 and line 616.
Line 669 – here you seem to imply that the two species DO overlap geographically in the exhibit? Yes? NO? this Is important if they can be back with their foster parents?
Overall, I would love to see more relevance to conservation issues. It is hinted to on line 708 – talking about the lack of self sustainability of captive populations. Is this relevant for conservation issues in the field? A stronger conservation message at the end would be great.
Comments for author File: 
Comments.pdf
Author Response
Reviewer 1
I would first like to state that this is perhaps one of the most thorough sets of data that I have experienced in a paper in my 30 years of science. Very impressive!!!
Thank you for the comment. We are pleased that you like the work.
After reading through the entire paper, here is my overall gestalt: The two species of flamingoes are really quite similar, and while the minimal differences between the two are well explained, the authors really state that the big difference is their phenotype/appearance (lines 117-19). Indeed, other potential differences, in my opinion, are also probably lessened given the pretty similar rearing conditions between the two groups, as opposed to had these been reared and then transferred to very different places. So, the control and experimental groups are very similar, really. Thus, after all is said and done, after the massive analysis, I am really not surprised that no major differences between foster and parent reared chicks were observed.
This lack of difference would have been more satisfying if there were data that were out there suggesting that this experimental set up might be really important, given a significant negative trend that has been observed. Indeed, there appears to be no literature, beyond the fact that Chilean flamingoes are more endangered, and this important to determine if a broader suite of husbandry practices could be useful, to suggest that husbandry, in general, of Chilean flamingoes is problematic. There are not references on success rates in other studies, if survival of Chilean flamingoes in captivity vary from other species, etc. I guess I am saying that a better set up of the conservational importance of this study would be warranted. It is a very very very complete analysis of behavior results of the two systems…but if the reason we do this is just because we happened to have this accidental cross-fostering event at the facility, is less compelling. If you make me more interested in why this might be of some pretty important conservational concern, then, at the end, I’ll be very happy that it seems like this example of an alternate rearing paradigm seems to be ok, and thus potentially beneficial for the conservation of this endangered species.
Thank you for the comments. This literature does not exist unfortunately. We’re explaining this as a husbandry intervention and not a conservation intervention. We’ve restructured our introduction to focus on the information that explains past attempts at cross fostering and fostering rearing and focussed specifically on avian examples.
We have attempted to explain why the differences are not as unexpected as claimed. Andean flamingos rarely breed in captivity and are rarely kept in captivity. We have included this as a known unknown. Hence why this cross fostering attempt was monitored.
Now I will return to the paper and work through some points as I move through it:
Introduction:
This paper is ultimately about parent rearing vs. cross-fostering of the Chilean flamingoes. The introduction got me a bit lost in the weeds, adding hand rearing, foster rearing, and peer-rearing, to the mix. There must be 100% clarity in the differences. Perhaps a better table defining what I think are the 5 possibilities that are variously brought up/discussed in the introduction...such as:
Parent reared – by mom and dad (which was done here)
Hand reared – by a human
Peer- reared – by same species with other chicks in brood
Fostered- reared = by same species with no other chicks in brood
Cross-fostered by DIFFERENT species (no idea about other chicks around??) also done here, correct?
Indeed, I think the definitions above are correct, but peer-reared, in particular is a bit confusing to me…. Is foster-rearing only reared by a same-species parent with no other chicks? Is peer-reared only same species? Is there a difference when you are cross-reared if your foster parents have other chicks or do cross-foster-parents never have chicks of their own species? These are the questions that came to mind as the authors worked through past studies of these different systems.
This comments relates to all of the above points. We have edited the definitions of the rearing conditions in the text. We have provided a reference for foster and cross foster rearing as key to what was performed in this research.
With a better definition/distinction of the different rearing types above, ultimately, perhaps some of my confusion in the introduction would be reduced, if terms are stuck to, and references are appropriately classified based on what types of rearing systems were studied.
As above. We have clarified the terms used.
Here is a specific example of my confusion: Paragraph starting on Line 74 “Indications that the early…..”, the numerous examples from the first part of the paragraph (sandhill cranes, moles, deer, etc.) all refer to cross-fostering studies (parents NOT of the same species). However, the final example of the Nene study (reference 44) appears to be a foster-rearing type study – with only Nene involved (granted, in different types of interaction between parents and chicks). Thus, the background comparison/set up for the experiment here (which is really a study of cross-fostering vs parent-reared study).
At the end of the day, the introduction would either benefit from a reduction to focus on parent- vs cross-fostering background studies alone, or a significant re-write to make sure the various other methods are defined well, and background studies compared consistently. I see how the latter can be frustrating, as I imagine the literature is a big mish-mash of comparisons between multiple rearing methodologies.
Lines 97-101: You say “authors have advised against, and limited, the use of fostering as a husbandry technique for reintroduction programs…”. Cross fostered? Regular fostered? Fostering in general? Is this a statement that unless you’re raised by your own mom and dad, it’s a problem?
Thank for the feedback. This comment relates to the above three comments. We have edited this entire section. Removed references and examples. We have now only focussed on specific related to the observations conducted.
Paragraph starting line 106: HERE is the place where it would be nice to have further discussion of the importance of this comparison beyond the ease in designing the study. I might even perhaps leave off or modify the sentence starting “Behavioral differences…” as you are basically saying that, since these two are so similar, we probably aren’t going to find differences……
We have explained that the lack of Andean flamingos in captivity means that we have no real benchmark on what to expect, similarities or differences wise in how the rearing might impact on long term chick development.
Methods:
I apologize if I missed some of these details.
- Are the two species kept separate in the exhibit? Flocks of Chilean and Andean flamingoes do NOT interact directly? This is important to establish….once the foster chicks are moved back, they have no chance to see their foster parent. This was not obviously stated. (See line 153 – describing where the Chilean flamingoes reside, but no mention of the Andean)
We have clarified details on where the birds were housed and where the chicks were housed at different stages.
- Observations: I’m confused between the scan sampling data and the photographic data. How did the two methods contribute to the variables measured? Were the behaviors from the ethogram determined from photos? From live watcher? This is unclear.
All behavioural data were obtained from photos taken at 5 minute intervals in the same manner as other flamingo research conducted by WWT. We have included more information and references.
- Statistical analyses: I have no competency to evaluate the appropriateness and or correctness of the statistical tools used in these analyses. I will assume that they are the correct methods to use to make these comparisons, and the statistical comparisons/tests used to compare the two groups of chicks is appropriate.
Results:
As stated above, I must say that this is a pretty impressive (perhaps daunting might be a more appropriate word) set of results. The details are Greek to me, and I wonder if the massive tables might be more appropriate as appendices or supplementary information, if those structures are available in the JZBG.
Thank you for the comment. We have edited the placement of tables in the main text to remove some to appendices.
Overall, the ability to glean results from a subset of the figures (#3, 4, 5 & 6) is 100% dependent on being able to see the paper in color. I, personally, prefer to still read papers on paper, and initially printed this in Black and White, which made it impossible for me to follow results well. This is perhaps not a fault of the author, but perhaps a concern for the Journal as a whole.
Thank you for the comment. We have attempted to change the colour scheme of some figures, but we followed the author guidelines that stated colour figures were appropriate.
Figures 3, 4b & 5: a better distinguishing line between the months would be helpful. (between the PAM and SHB of each month). Additionally, it is interesting that the foster chicks are all represented individually (and no comparison/distinguishing of sex of the 6 of them) and then compared to the groups of female and male parent-reared chicks. Would a summary bar of the 6 foster chicks, compared then to the parent-reared chicks be more informative? Would you see any differences more readily? I often find pause when individual data (i.e., the 6 foster chicks) are put out, when it is the GROUP data that we are concerned about. I guess my point is that, beyond the differences in how the different behaviors vary from top to bottom, the comparisons between groups of birds is less compelling.
Thank you for the comment. We have edited the figures for clarity as per your suggestions and we have included a foster chick average for comparison too.
Figure 4: If color is the go-to here, note that the description of colors in the caption of figure 4A (gray scale) are not consistent with the GREEN scale in the color figure.
We have edited this figure to improve the colour scheme and corrected the caption accordingly.
DISCUSSION:
Might the discussion begin with a version of the paragraph starting at 634. I think it would be nice to know at the start of the discussion that there appears to be no major issues between Chilean flamingo chicks reared by Andean parents or their own Chilean parents.
Edited accordingly.
Then, perhaps, the more detailed differences can be discussed.
Grammar issue line 610 and line 616.
Edited and reworded.
Line 669 – here you seem to imply that the two species DO overlap geographically in the exhibit? Yes? NO? this Is important if they can be back with their foster parents?
In exhibit not the wild, but based on the wild. We have edited to explain we are referring to the biologically relevant features of the enclosure.
Overall, I would love to see more relevance to conservation issues. It is hinted to on line 708 – talking about the lack of self sustainability of captive populations. Is this relevant for conservation issues in the field? A stronger conservation message at the end would be great.
We have attempted to add in a note regarding improved population sustainability. More evidence based cross fostering approaches could be useful for the future.
Reviewer 2 Report
Rev
I read this manuscript with very interest. Paper is well written with a very large amount of data and a strong statistical analysis. Moreover this type of research may provide useful information to carry out operational actions for management and conservation of this species. The behavioural approach is still poor used in this regard. In some countries there is a criticism about the zoological gardens. Do your data can provide support to the role of zoos? I would read in conclusions some sentences in this regard. However a good paper. I suggest to Accept it with only minor revisions. For example, in conclusions, can you provide some example from literature? Can you provide exaple of implication for conservation of your results? Minor suggestion: in row 72-73: ‘Lonchura striata var. domestica’ should be with ‘var’ not in italic.
In acknowledgments add the role anonymous reviewers and Editors.
Have a nive work.
Comments for author File: Comments.pdf
Author Response
Reviewer 2
I read this manuscript with very interest. Paper is well written with a very large amount of data and a strong statistical analysis. Moreover this type of research may provide useful information to carry out operational actions for management and conservation of this species. The behavioural approach is still poor used in this regard. In some countries there is a criticism about the zoological gardens. Do your data can provide support to the role of zoos? I would read in conclusions some sentences in this regard. However a good paper. I suggest to Accept it with only minor revisions. For example, in conclusions, can you provide some example from literature? Can you provide exaple of implication for conservation of your results? Minor suggestion: in row 72-73: ‘Lonchura striata var. domestica’ should be with ‘var’ not in italic.
We have attempted to include relevance of fostering to ex situ conservation efforts.
We have edited the scientific name accordingly
In acknowledgments add the role anonymous reviewers and Editors.
We have added extra “thank yous” to the acknowledgements.
Have a nice work.
Reviewer 3 Report
This is an interesting and well considered study, with a resulting paper that is well organized and impressively (if anything, perhaps over thoroughly) put together. The work is timely and extremely well justified, and the questions it raises about cross-fostering, and fostering in general, within captive species are quite interesting.
The execution and analyses of the study seem thoughtful and appropriate and I have no major critiques of these. As a minor point the authors might consider putting some of the tables and charts into an appendix, as wading through them was somewhat onerous. But it isn't a big deal.
The only issue I have with the study is in the description of the enclosure and how that relates to the interpretation of results. On a first read-through I misunderstood and assumed that flocks of each species were housed in separate locations at WWT Slimbridge. This led to confusion in interpreting the results, specifically concern that the different locations might present a confound based on experience with housing during observation. On second read through I recognized that the species were housed together, so every bird had roughly equivalent experience with the containment spaces, regardless of their rearing species. I think it might be worth it just to throw in a sentence or two explicitly explaining that, to help casual readers avoid the confusion I experienced.
One additional small note: there is a typo in the caption for figure 7. Should say "Best fitting" instead of "Bets fitting"
Author Response
Reviewer 3
This is an interesting and well considered study, with a resulting paper that is well organized and impressively (if anything, perhaps over thoroughly) put together. The work is timely and extremely well justified, and the questions it raises about cross-fostering, and fostering in general, within captive species are quite interesting.
The execution and analyses of the study seem thoughtful and appropriate and I have no major critiques of these. As a minor point the authors might consider putting some of the tables and charts into an appendix, as wading through them was somewhat onerous. But it isn't a big deal.
We have edited down the number of tables accordingly and we have clarified some of the findings presented in figures.
The only issue I have with the study is in the description of the enclosure and how that relates to the interpretation of results. On a first read-through I misunderstood and assumed that flocks of each species were housed in separate locations at WWT Slimbridge. This led to confusion in interpreting the results, specifically concern that the different locations might present a confound based on experience with housing during observation. On second read through I recognized that the species were housed together, so every bird had roughly equivalent experience with the containment spaces, regardless of their rearing species. I think it might be worth it just to throw in a sentence or two explicitly explaining that, to help casual readers avoid the confusion I experienced.
We have edited the methods to clarify the housing of the flocks and to show how chicks were moved between flocks. We hope this answers your concerns here.
One additional small note: there is a typo in the caption for figure 7. Should say "Best fitting" instead of "Bets fitting"
Thank you. We have edited this.
