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Article
Peer-Review Record

Mitigating Acute Climate Change Threats to Reintroduced Migratory Northern Bald Ibises

Conservation 2024, 4(4), 748-761; https://doi.org/10.3390/conservation4040044
by Johannes Fritz 1,*, Markus Unsoeld 2, Bernhard Goenner 3, Regina Kramer 3, Lisbet Siebert-Lang 3 and Helena Wehner 1
Reviewer 1: Anonymous
Reviewer 2:
Reviewer 3: Anonymous
Conservation 2024, 4(4), 748-761; https://doi.org/10.3390/conservation4040044
Submission received: 2 September 2024 / Revised: 16 November 2024 / Accepted: 19 November 2024 / Published: 2 December 2024

Round 1

Reviewer 1 Report

Comments and Suggestions for Authors

 

General comments:

Reintroduced Northern Bald Ibises (Geronticus eremita) breed both north and south of the Alps and migrate to a common wintering ground in Tuscany. Recently, they could not cross the Alps and remain in the northern Alpine foothills without sufficient thermals owing to the delay of autumn migration. This research reported the project of the establishment of a second migration route to a wintering area in Andalusia, Spain, connecting with a sedentary population there. It is a very meaningful work, and the manuscript is well written.

Special comment:

 There is too much repetition in the discussion and results section, and it is suggested to simplify the discussion section.

 

 

Author Response

General comments: Reintroduced Northern Bald Ibises (Geronticus eremita) breed both north and south of the Alps and migrate to a common wintering ground in Tuscany. Recently, they could not cross the Alps and remain in the northern Alpine foothills without sufficient thermals owing to the delay of autumn migration. This research reported the project of the establishment of a second migration route to a wintering area in Andalusia, Spain, connecting with a sedentary population there. It is a very meaningful work, and the manuscript is well written.

Reply: Thank you for the general, positive evaluation of our manuscript.

 

Special comment: There is too much repetition in the discussion and results section, and it is suggested to simplify the discussion section.

Reply: We have revised the discussion, shortened it and removed repetitions.

Reviewer 2 Report

Comments and Suggestions for Authors

The guidance of birds during their first migration is a remarkable event because of its technical difficulty and the possibility of obtaining individualised information on the migration costs of birds. This paper presents the case of the Ibis (Geronticus eremita) in its first autumn migration from Germany to southern Spain. It also provides a wealth of information on the migration across the Alps between 2011 and 2013. The storytelling of the text is interesting.

Some aspects of the manuscript have room for improvement. For example, it is not sufficiently explained that for most medium and large bird species, autumn migration includes sites where birds stay for long periods, as opposed to spring stopovers where their stay is usually much shorter. The manuscript needs to comment on the duration of migration stopovers under natural conditions: are stopovers limited to strict night roosting (stopover sites)? Are they longer and variable according to the resources available (staging sites)?  In the experiment, however, the duration of autumn stopovers was that of a short staging site. How will this first experience affect subsequent migrations? Both in terms of building up body reserves and finding adequate food. In the experiment, the ibises did not learn to feed at the stopover sites. Or did they? Please explain this key point in the text. The same birds should use the same sites during their second autumn migration. Do you plan to set up feeding stations at each of the 19 stopover sites of the first autumn migration (Figure 6)?  Also, this species is typical of wetlands, yet the manuscript does not explain whether the night stops were placed near wetlands.

There is little information on the characteristics of the staging points. It is essential to improve the manuscript by explaining the characteristics of the staging areas and their concordance with natural sites (available food, shelter, roosts, water, etc.). The discussion should explain the consequences for ibis survival of the characteristics of the areas chosen as autumn roosting sites. The manuscript must also include information on the amount of food provided so that weight change can be assessed (lines 216-221). It is not sufficient to report weight change without specifying the type and amount of food received at the stopover sites. If this topic has been the subject of another publication, please indicate this in the main text.

Since 2016, most birds are equipped with GPS devices (line 130). It is therefore possible to describe the migration phenology with its three statistical data: the 10% quantile, the median or 50% quantile and the 90% quantile.  The onset date of the first bird may not be representative due to the lack of repeatability of one subject. How is the onset date calculated? This is not explained in the methods. The median date is the day of the year when half of the marked birds have started to migrate and half have not yet started to migrate. The median date is the statistical standard because of the enormous variation in migration phenology, for example due to weather conditions. To improve the manuscript, the same analyses (lines 183 - 191) could be calculated using the median migration onset dates.

Individuals are mostly marked with GPS devices since 2016, so the random factor "subject" needs to be included in analyses of migratory phenology in recent years. Basic questions such as which individual is represented in Figure 4 can be answered. Other more far-reaching questions, such as what is the inter-annual repeatability of migration onset in each individual equipped with tags and GPS device, can also be answered. Perhaps the regression line (line 185) is repeatable between individuals. Perhaps females and males migrate on different dates. The latter is unlikely in the first autumn migration but possible in the spring, depending on the species. Since it is their first migration, sexual differences should not be apparent yet. But this assumption must be confirmed statistically.

The manuscript is not clear enough in stating how many datasets will be analysed and what questions each dataset will answer. For example, data on migrations across the Alps and data on migrations (or migrations) along one side of the Pyrenees. The twelve years of migration are analysed together (e.g. line 183), but most birds do not have GPS tags in every year.

Birds return to their place of birth in their third year (line 127), so the autumn migration of the breeding population is not, or may not be, composed entirely of birds in their first year. What is the migration phenology of individuals older than three years? As the study covers 12 years, spring and autumn migration of individuals older than 3 years must have been observed at least on the onset (departure) and arrival dates. The manuscript should comment on this part of the population, how they migrate and whether individuals that have followed a human across the Alps then follow these other individuals.

Were the birds sexed? This should have been done using molecular techniques. The manuscript should explain in the methods why they were not sexed. If they were, it should be explained why this factor is not analysed in this paper. Individuals from zoos may have been sexed. It is strange that a wildlife reintroduction programme would release unsexed individuals. Justify the lack of sexing in the revised manuscript and how this lack of sexing can determine the failure of the reintroduction program. In fact, sex differences in daily weight changes during migration could be analysed.



Minor comments

Lines 222-224. The last paragraph (lines 222-224) does not seem to be a result. Perhaps a note on how to present it.


Lines 344-345. The future will show what kind of dynamics result from the diversity and large-scale distribution of migratory and sedentary colonies. Of course, because that's the only way it will happen. This sentence contains what is known as a truism, which is a statement that can only be true. The sentence can be rewritten in a style that does not state the obvious.  For example: "We expect that diversity and large-scale distribution of migratory and sedentary colonies will increase the ecological flexibility of the population."

Please check the format and details given in the references. Some examples:

Lines 379-381. The year is 2017, not 2016. Add volume 27 and pages 537-549

Line 384. Remove the publisher name Elsevier

Line 397. Add article number 891079 after volume 10

Line 399. Style: remove the comma in 'Society, Interface'

Line 401. Style: the scientific name of the ibis should be formatted in italics.

Line 440. Insert the volume number of the journal Oryx


Author Response

Comment 1: The guidance of birds during their first migration is a remarkable event because of its technical difficulty and the possibility of obtaining individualised information on the migration costs of birds. This paper presents the case of the Ibis (Geronticus eremita) in its first autumn migration from Germany to southern Spain. It also provides a wealth of information on the migration across the Alps between 2011 and 2013. The storytelling of the text is interesting.

Reply: We thank Reviewer 2 for the positive overall assessment. Just to clarify, human-led migrations from different sites in the northern foothills of the Alps to southern Tuscany took place not only from 2011 to 2013, but from 2004 to 2022 with a total of 15 migrations (line 179).  

Comment 2: Some aspects of the manuscript have room for improvement. For example, it is not sufficiently explained that for most medium and large bird species, autumn migration includes sites where birds stay for long periods, as opposed to spring stopovers where their stay is usually much shorter. The manuscript needs to comment on the duration of migration stopovers under natural conditions: are stopovers limited to strict night roosting (stopover sites)? Are they longer and variable according to the resources available (staging sites)?  In the experiment, however, the duration of autumn stopovers was that of a short staging site. How will this first experience affect subsequent migrations? Both in terms of building up body reserves and finding adequate food. In the experiment, the ibises did not learn to feed at the stopover sites. Or did they? Please explain this key point in the text. The same birds should use the same sites during their second autumn migration. Do you plan to set up feeding stations at each of the 19 stopover sites of the first autumn migration (Figure 6)?  Also, this species is typical of wetlands, yet the manuscript does not explain whether the night stops were placed near wetlands.

Reply: Since the focus of this paper is mainly on the human-led migration and the mitigation measures against climate change we did not focus in detail on the migration pattern of the release population, e.g. on stopover patterns and comparison between spring and autumn migration. There is a further paper in preparation, which comprises extensive quantitative analyses regarding the migratory behaviour of the wild population. It turns out that the behaviour of the wild Northern Bald Ibises corresponds to the general patterns of spring and autumn migration. But we would like to reserve these results for the next paper. However, in this current paper we added the mean duration of stopovers during the human-led migrations to Tuscany (line 187) and the initial human-led migration to Andalusia (line 253) and also added a regarding sentence in the method section, explaining that the duration of stopovers ranges from mere night stays to extended stays of a week or more (line 127-128).  In the method section we also added a paragraph where we explain, what we feed to the birds and that they are fed by the foster parents throughout the human-led migration (line 129-137). In the discussion we added a paragraph where we explain that after rewilding the reintroduced birds usually do not migrate along the route they flew on with the ultralight aircraft and that they only occasionally use the stopovers we landed with them on during the human-led migration (line 416-418). Due to that and also because it interferes with the goal of a self-sustaining population, we do not plan to set up feeding stations, neither on the breeding or wintering sites nor along the flyway. The species has no affinity for wetlands, rather to meadows, pastures and semiarid landscapes (line 130/131), therefore we did not place stopovers near wetlands.


Comment 3:
There is little information on the characteristics of the staging points. It is essential to improve the manuscript by explaining the characteristics of the staging areas and their concordance with natural sites (available food, shelter, roosts, water, etc.). The discussion should explain the consequences for ibis survival of the characteristics of the areas chosen as autumn roosting sites. The manuscript must also include information on the amount of food provided so that weight change can be assessed (lines 216-221). It is not sufficient to report weight change without specifying the type and amount of food received at the stopover sites. If this topic has been the subject of another publication, please indicate this in the main text.

Reply: Stopovers during the human-led migration were chosen not primarily from the perspective of potentially suitable future stopover areas for the Northern Bald Ibis, but rather the flight suitability and the availability of suitable infrastructure for the camp. This is justified by the finding that reintroduced birds usually do not migrate along the route they flew on with the ultralight aircraft and only occasionally use the stopovers we landed with them on during the human-led migration (line 416-418), in conjunction with the evidence for the ample availability of suitable foraging areas (see Wehner et al. 2022). We added corresponding passages to the results (line 183-186) and in the discussion (line 422).
We added a paragraph regarding the type and amount of food received at the stopover sites (line 134-137).

Comment 4: Since 2016, most birds are equipped with GPS devices (line 130). It is therefore possible to describe the migration phenology with its three statistical data: the 10% quantile, the median or 50% quantile and the 90% quantile.  The onset date of the first bird may not be representative due to the lack of repeatability of one subject. How is the onset date calculated? This is not explained in the methods. The median date is the day of the year when half of the marked birds have started to migrate and half have not yet started to migrate. The median date is the statistical standard because of the enormous variation in migration phenology, for example due to weather conditions. To improve the manuscript, the same analyses (lines 183 - 191) could be calculated using the median migration onset dates.

Reply: We are aware that the median is the usual presentation, but the data in the period from 2011 to 2015 and partly beyond are purely observational data and therefore we have decided on this analysis and would like to keep it. We would also like to make it clear that the beginning is not an individual but the first group, which consists of at least 2 individuals. To clarify how we calculated the onset we added a section in the methods (line 152-161) and we extended the regarding section in the results (line 221-228).

Comment 5: Individuals are mostly marked with GPS devices since 2016, so the random factor "subject" needs to be included in analyses of migratory phenology in recent years. Basic questions such as which individual is represented in Figure 4 can be answered. Other more far-reaching questions, such as what is the inter-annual repeatability of migration onset in each individual equipped with tags and GPS device, can also be answered. Perhaps the regression line (line 185) is repeatable between individuals. Perhaps females and males migrate on different dates. The latter is unlikely in the first autumn migration but possible in the spring, depending on the species. Since it is their first migration, sexual differences should not be apparent yet. But this assumption must be confirmed statistically.

Reply: We fully agree that further analysis on the phenology of spring and autumn migration are worth doing and we refer to the already mentioned paper in preparation, which deals with that. However, in our view, these further analyses are not the subject of this paper. Figure 4 does not refer to individual but the first group that initiates the autumn migration each year, whereby the group consists of at least two individuals. We have added information on this in the results (line 228-232). Regarding the composition of these groups (age and sex) we added further analysis to the results (line 226-228).

Comment 6: The manuscript is not clear enough in stating how many datasets will be analysed and what questions each dataset will answer. For example, data on migrations across the Alps and data on migrations (or migrations) along one side of the Pyrenees. The twelve years of migration are analysed together (e.g. line 183), but most birds do not have GPS tags in every year.

Reply: The main analysis regards the migration to Tuscany in the years from 2011 to 2023. We added a section to the methods, where this is now clearly stated (line 157-161). For the migration to Andalusia, we just described the phenology in the section of the results (line 249-2&6). 

Comment 7: Birds return to their place of birth in their third year (line 127), so the autumn migration of the breeding population is not, or may not be, composed entirely of birds in their first year. What is the migration phenology of individuals older than three years? As the study covers 12 years, spring and autumn migration of individuals older than 3 years must have been observed at least on the onset (departure) and arrival dates. The manuscript should comment on this part of the population, how they migrate and whether individuals that have followed a human across the Alps then follow these other individuals.

Reply: The autumn migration always consists of either only experienced subadult or adult migrants or of mixed groups which consist of experienced migrants and juveniles. A general description of this phenology is in the introduction (line 65-68). Information on the composition of the groups is now added to the results (line 226-228). A juvenile needs to learn once the route to the wintering site, either by following an experienced conspecific or a foster parent in the microlight. Therefore, a bird which followed the microlight does not have to follow a conspecific later on. However, they later on lead wild born juveniles.

Comment 8: Were the birds sexed? This should have been done using molecular techniques. The manuscript should explain in the methods why they were not sexed. If they were, it should be explained why this factor is not analysed in this paper. Individuals from zoos may have been sexed. It is strange that a wildlife reintroduction programme would release unsexed individuals. Justify the lack of sexing in the revised manuscript and how this lack of sexing can determine the failure of the reintroduction program. In fact, sex differences in daily weight changes during migration could be analysed.

Reply: All birds were sexed (line 107-108).

Minor comments

Lines 222-224. The last paragraph (lines 222-224) does not seem to be a result. Perhaps a note on how to present it.

Reply: Indeed, we modified the discussion accordingly and deleted this paragraph. 

Lines 344-345. The future will show what kind of dynamics result from the diversity and large-scale distribution of migratory and sedentary colonies. Of course, because that's the only way it will happen. This sentence contains what is known as a truism, which is a statement that can only be true. The sentence can be rewritten in a style that does not state the obvious.  For example: "We expect that diversity and large-scale distribution of migratory and sedentary colonies will increase the ecological flexibility of the population."

Reply: Thanks, we fully agree and changed it accordingly (line 441-442).

Please check the format and details given in the references. Some examples:

Lines 379-381. The year is 2017, not 2016. Add volume 27 and pages 537-549

Line 384. Remove the publisher name Elsevier

Line 397. Add article number 891079 after volume 10

Line 399. Style: remove the comma in 'Society, Interface'

Line 401. Style: the scientific name of the ibis should be formatted in italics.

Line 440. Insert the volume number of the journal Oryx

Reply: Thank a lot you for the thorough revision of the bibliography, we changed it accordingly.

 

Reviewer 3 Report

Comments and Suggestions for Authors

Dear Authors,

I have completed my review of your very interesting manuscript on Northern Bald Ibises and thoroughly enjoyed reading it. Overall, the manuscript is well-written, well-organized, and certainly deserves to be published. However, I have a few comments that I would like the authors to consider while revising their text.

Firstly, I believe the closing of the introductory section could be strengthened. Please clearly and directly state your objectives. You are not just "reporting on the introduction" of the species so far—you have accomplished much more than that.

I also recommend reorganizing the discussion section (as detailed below). The focus should be on your data and analysis, which are compelling. For instance, the initial paragraphs of the discussion repeat content from the introduction. Concentrating on your results would enhance the flow and impact of the discussion.

Below are a few minor comments:

Lines 33-35: If I understand correctly, the authors state that the species historically bred along the Mediterranean and spent the non-breeding season in two different areas in Africa. However, the migratory component is not explicit. I suggest being more straightforward and stating that the historical breeding area of the species was in southern Europe, and after breeding, the birds migrated to Africa.

Lines 36-38: "Extirpation" is a more accurate term than "extinction" here, similar to the terminology used in the first paragraph.

Line 63: The same comment applies as above.

Lines 137-138: It would be helpful to elaborate on your data analysis methods. Please inform the readers of the specific analysis tests you performed, why they were chosen, and for what purpose.

Lines 226-244: Much of the content in these two paragraphs either repeats information from the introduction or could be moved there. I recommend starting the discussion with a summary of your main findings and then proceeding to discuss your data in the context of the previous literature. In fact, your discussion really begins in the third paragraph, where you start engaging with your data.

Comments on the Quality of English Language

English of the manuscript is generally good, with only minor revisions needed after the authors revise the text. Most of these revisions can be addressed during the copy-editing process.

Author Response

General Comment: I have completed my review of your very interesting manuscript on Northern Bald Ibises and thoroughly enjoyed reading it. Overall, the manuscript is well-written, well-organized, and certainly deserves to be published. However, I have a few comments that I would like the authors to consider while revising their text.

Reply: Dear Reviewer, we thank you for the positive overall assessment of our manuscript and the very helpful comments.

Comment 1: Firstly, I believe the closing of the introductory section could be strengthened. Please clearly and directly state your objectives. You are not just "reporting on the introduction" of the species so far—you have accomplished much more than that.

Reply: We changed the final paragraph of the introduction accordingly (line 89-92).

Comment 2: I also recommend reorganizing the discussion section (as detailed below). The focus should be on your data and analysis, which are compelling. For instance, the initial paragraphs of the discussion repeat content from the introduction. Concentrating on your results would enhance the flow and impact of the discussion.

Reply: Thank you for this note and the following specific comments. We have shortened and focussed the discussion.

Below are a few minor comments:

Lines 33-35: If I understand correctly, the authors state that the species historically bred along the Mediterranean and spent the non-breeding season in two different areas in Africa. However, the migratory component is not explicit. I suggest being more straightforward and stating that the historical breeding area of the species was in southern Europe, and after breeding, the birds migrated to Africa.

Reply: This paragraph was rather misleading. Actually, the historic wintering site(s) for the European population is unknown, but archaeological findings indicate a flyway along the Mediterranean coast to Gibraltar (and probably further to Africa). We modified the paragraph accordingly (line 33-39).

Lines 36-38: "Extirpation" is a more accurate term than "extinction" here, similar to the terminology used in the first paragraph.

Line 63: The same comment applies as above.

Reply: We fully agree and changed the term in all places accordingly (line 30,40,69,348,372)

Lines 137-138: It would be helpful to elaborate on your data analysis methods. Please inform the readers of the specific analysis tests you performed, why they were chosen, and for what purpose.

Reply: We have expanded the paragraph accordingly (line 152-161, 163-167).

Lines 226-244: Much of the content in these two paragraphs either repeats information from the introduction or could be moved there. I recommend starting the discussion with a summary of your main findings and then proceeding to discuss your data in the context of the previous literature. In fact, your discussion really begins in the third paragraph, where you start engaging with your data.

Reply: We have thoroughly revised and structured the discussion. The first two paragraphs were deleted.

Round 2

Reviewer 2 Report

Comments and Suggestions for Authors

The majority of the problems have been resolved in the second edition of the manuscript. As the authors state in the response text, other aspects that have not been extensively analysed will be addressed in future manuscripts. It is clear that further important aspects for the conservation of this species, such as the parameterisation of population dynamics (survival and fecundity of male and female birds using the new migration route), will require the expansion of the individual database through more years of field research on the Northern Bald Ibises. Given the inevitability of waiting for a good number of years, it can be accepted that the present manuscript provides sufficient information for the conservation of these ibises.  In addition, this information can be used to justify the long-term continuation of the conservation plan.

Minor comment:

Revise the following sentence (lines 224-226): "Even though the size of the group which initiated the autumn migration varied considerably, it has not increased significantly over the years (linear model, R²=0.4661, p=0.0144)". The statistical result (p<0.05, significant effect) contradicts the statement "not increased significantly". Please clarify the discrepancy. It may be a simple typographical error.

 

 

 

Author Response

We would like to thank again for the comprehensive and very qualified comments, the revision based on them has greatly improved the quality of the manuscript.

The parameterisation of population dynamics will be in the focus of further analyses, and we hope to benefit again from such qualified reviews of our manuscripts.

Minor comment:

we changed the sencence as follows:
The size of the group which initiated the autumn migration varied considerably, with a slightly increasing group size over the years (Linear Model, R²=0.4661, p=0.0144). 

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