Grassland Alterations Do Not Affect Breeding Success, but Can Explain Dietary Shifts of a Generalist Raptor Species
Round 1
Reviewer 1 Report
This study focuses on the dietary shifts of the Eastern Imperial Eagle and investigates quite thoroughly its relation to land use changes and grassland loss in particular. The text is well written with plenty of information on the relevant topic. In addition, the available dataset is sufficient for analysis and the statistical procedure followed by the authors is adequate for the purpose of the study. Overall, I believe that the study is valuable on the topic of raptor ecology and certainly merits publication.
I have only general comments that would clarify and improve the manuscript, although I realize that connection habitat alteration, dietary shifts, and reproductive success is not an easy task.
- First in the “Abstract” section, the authors should avoid presenting statistical figures or p-values. They should stay on the results without mentioning any mathematical evidence. This has been achieved successfully in the text.
- Second, the text needs some reforming apart from font size (for instance font size is inconsistent in lines 45-50, 58-60 and elsewhere).
- In the “Material & Methods” section, I would suggest some restructuring. All spatial data acquired from CLC database or percentages of habitat types within eagle territories should be presented in one sub-section. Then, another sub-section should refer to the fieldwork procedures e.g. diet data collection and analysis. Actually some details are missing namely: Was the diet analysis based on direct observation of prey deliveries during nest guarding or it was based on identification of prey remains/ pellets? (Please clarify that).
- Furthermore, the figures needs some improvement. They must be optically simple and comprehensible. In Figure 2, avoid the indication “X” in the mean-lines of the box-plots. In Figure 3, avoid double decimals in X labels as well as the x indication in the bars and the asterisk in the Y labels. The asterisk (*) for significant differences should better be placed on the top of the bars, or the significant prey categories should be pinpoints in bold. In the present form, figures are over-stated.
- Similarly, in Table 2, I do not see any particular point to present territorial diet differences. The diet comparison between the two time-periods is the main issue here.
- In Figure 4, only the significant relationships should remain. There is no need to present everything. Relevant comments have been nicely included in the text.
- Last but most importantly, the “Discussion” section needs some structural improvement with clear paragraphs and simple but concise comments. For instance how the authors explain that in an eagle territory the consumption of sousliks was 4.7 times more likely, although the pastureland had decreased by 50%. Moreover, why the (random) territory effect was a more powerful factor in shaping the dietary response of EIE to habitat changes. Perhaps an interaction term of territory*time-periods should be examined in the GLM models.
- The reproductive success issue is quite important and I would suggest some more data on that. Are there any indirect data (e.g. territory occupancy, pair composition i.e. mixed adult-sub adult mates) that would imply the age/ experience of the breeding pairs?
- Is it likely that the dietary shift of the target species is a product of a change in the eagles’ foraging range? I admit that this is difficult estimate, but food energy intake would be higher if the eagles hunt storks in a nearby farmland, or garbage dump than over a natural grassland. I would suggest that the main four prey items (i.e. hedgehog, brown hare, souslik and white stork) were connected with the EIE foraging range and commented respectively in the “Discussion” section. Perhaps, territory quality in terms of foraging budgets provide a clue on the higher breeding success in the after grassland-loss period.
Author Response
Reviewer 1
Dear Reviewer,
Thank you for your positive feedback and comments. We considered all of them important and consequently addressed everything you pointed out. You can find below our replies to each comment done by you:
Reviewer 1: First in the “Abstract” section, the authors should avoid presenting statistical figures or p-values. They should stay on the results without mentioning any mathematical evidence. This has been achieved successfully in the text.
Authors response: Done.
Reviewer 1: Second, the text needs some reforming apart from font size (for instance font size is inconsistent in lines 45-50, 58-60 and elsewhere).
Authors response: Done. This resulted because of the system upload.
Reviewer 1: In the “Material & Methods” section, I would suggest some restructuring. All spatial data acquired from CLC database or percentages of habitat types within eagle territories should be presented in one sub-section. Then, another sub-section should refer to the fieldwork procedures e.g. diet data collection and analysis. Actually some details are missing namely: Was the diet analysis based on direct observation of prey deliveries during nest guarding or it was based on identification of prey remains/ pellets? (Please clarify that).
Authors response: Done. We added and clarified the information between lines 169 and 181. Generally, we haven’t based our diet analysis on direct observations but only from the collected material. Check the text.
Reviewer 1: Furthermore, the figures needs some improvement. They must be optically simple and comprehensible. In Figure 2, avoid the indication “X” in the mean-lines of the box-plots. In Figure 3, avoid double decimals in X labels as well as the x indication in the bars and the asterisk in the Y labels. The asterisk (*) for significant differences should better be placed on the top of the bars, or the significant prey categories should be pinpoints in bold. In the present form, figures are over-stated.
Authors response: Done. We amended Fig.2. In fig.3 we amended the figure but didn’t bald the significant labels and just left the asterisk (*) not to overstate the figure again like you mentioned.
Reviewer 1: Similarly, in Table 2, I do not see any particular point to present territorial diet differences. The diet comparison between the two time-periods is the main issue here.
Authors response: But we present the Results of the over-parameterized linear model (GLM) carried out to analyze the trend of the different prey categories (frequency and biomass contribution). In this model, Territory was included as a “Random” factor, Period (before change: 2001-2010; after change: 2012-2021) and period was included as a “Fixed” factor. Therefore, by removing the territory from the table we will actually not present the entire analysis result. We thus think this should remain as it is now.
Reviewer 1: In Figure 4, only the significant relationships should remain. There is no need to present everything. Relevant comments have been nicely included in the text.
Authors response: We removed the figure entirely because of the other reviewer’s comments.
Reviewer 1: Last but most importantly, the “Discussion” section needs some structural improvement with clear paragraphs and simple but concise comments. For instance how the authors explain that in an eagle territory the consumption of sousliks was 4.7 times more likely, although the pastureland had decreased by 50%. Moreover, why the (random) territory effect was a more powerful factor in shaping the dietary response of EIE to habitat changes. Perhaps an interaction term of territory*time-periods should be examined in the GLM models.
Authors response: We added a sentence to clarify this it’s highly significant which part of the territory is altered. However, it’s highly significant which part of the territory is altered. For example, an eagle territory might be largely destroyed but the souslik colony remains unharmed and its population increases.
Reviewer 1: The reproductive success issue is quite important and I would suggest some more data on that. Are there any indirect data (e.g. territory occupancy, pair composition i.e. mixed adult-sub adult mates) that would imply the age/ experience of the breeding pairs?
Authors response: We have analysed this in lines 512-519: Furthermore, the age of breeding birds is another important factor driving the reproduction of large raptor species (Balbontín et al. 2003, Ferrer, Bisson 2003, Margalida et al. 2008). It was documented that pairs of adult EIE’s had significantly bigger breeding success than immature birds involved in reproduction (Horváth et al. 2014). In our study, 21.07% of the breeding eagles were in immature plumage in the pre-alteration period, against to only 6.58% immature breeders in the years after habitat transformation in the same focal territories. Adult eagles gain more experience and successfully raise more progeny (Margalida et al. 2008, Horváth et al. 2014).
Reviewer 1: Is it likely that the dietary shift of the target species is a product of a change in the eagles’ foraging range? I admit that this is difficult estimate, but food energy intake would be higher if the eagles hunt storks in a nearby farmland, or garbage dump than over a natural grassland. I would suggest that the main four prey items (i.e. hedgehog, brown hare, souslik and white stork) were connected with the EIE foraging range and commented respectively in the “Discussion” section. Perhaps, territory quality in terms of foraging budgets provide a clue on the higher breeding success in the after grassland-loss period.
Authors response: Because our territorial eagles were not fitted with transmitters before and after grasslands transformations, we can’t evaluate the utilization change in their territory. On the other hand, we have a large data set that we have analyzed describing the main foraging behaviour tendencies and their adaptation to a more specified food like hedgehogs and storks and the respective food niche breadth decrease. In respect to territory quality effect, we have already published a paper. Our results show that habitat alterations reduce territory quality. Furthermore, out of our 15 focal territories, 14 are of high quality that makes the comparison impossible (In respect to territory quality effect).
Reviewer 2 Report
The whole paper, especially the methods, and results, is tough to follow and needs to be rewritten due to a dire need to improve the English.
There is something bizarre with the font size, which varies throughout the MS. Maybe, I received the MS after a review? However, the font must be consistent throughout and follow the journal's requirements. Also, the references style did not follow the template.
There is an overall problem with the concept of the paper. In Figure 4 shows that there were no relationships between the proportion of grassland change and the proportion of different prey change (shift). Does this mean that the changes in Figure 3 were caused by something other than grasslands? If this is the case, then is kind of undermind the title and the paper's purpose. Is the title correct? According to the data, it is not. Maybe I missed something. Also, in Figure 6: the breeding success increased after a decrease in grasslands. This also goes against the idea that habitat change is bad. The sample size is large and good, but the results do not always accompany the introduction and discussion and should be rewritten accordingly.
Abstract:
Line 13: Please add the Latin name.
Line 18: Raptors do not forage on prey but predate, hunt, or prey on prey.
Lines 16-23:This section is too wordy. Maybe state that prey species were eaten more and four species less the after the transformation
Lines 24-29: If diet affects breeding, why was breeding not affected by the grassland alternation? If the goal is to determine whether grassland alteration affects the breeding and diet of the eagles, and the authors state in the title that the grassland alterations do not affect breeding, then I am not sure how these sections fit in the MS?
This section should be shortened.
Lines: 34-38: If breeding was not affected, why should grasslands be preserved? I am unsure how these recommendations fit within the results of this study.
Lines 45-48: Is this true? Are there not other natural habitats other than grassland?
Lines 45- 49? I would add citations
Line 66: What about providing new prey species? For example, agricultural pest species.
Line 70-72: This does not make sense. Or, more likely, you provide one option only. For example, if they adapt their behavior by switching prey species, they may also increase reproduction or reproduce similarly.
Lines 82-84: Rewrite Unclear. English
Lines 92- 96- Rewrite. English
Lines 97-100. Unclear why this is important. Maybe move to the next paragraph
Lines 100- 103- Rewrite. English
Lines 117-120: Rewrite, English.
Lines 122-1385 English, kind of hard to follow/
137: Study Design
138:161: Rewite hard to understand. Also, where in Bulgaria? Size of study site? During what years? Etc et…. Missing basic information about the study site.
141-145: Different types of grasslands? What types?
148-153: Rewrite into one sentence. Also, what about the two periods? We compared "?" (breeding and diet between two periods?
Lines 151-152: What habitat analysis?
Line 154: What is this link? It does not work
154-145: In both cases? What cases?
It is unclear the use of the "first step" ( line 138) and "second step" (line 168).
Lines 162-167. Why is this section not in the second step of the diet analysis?
Lines 183-185: Rewrite: English
Lines 185-188: Hard to follow. Isn't this written above in lines 164-166?
189L English
Line 190-191: You write above< "breeding pairs" now you use "incubating pair".
Lines 191-193: Needs to be rewritten (English).
206: To avoid , "Pseudoreplication"
Line 208: Were the eagles ringed? If not state it.
Lines 208-213: English
You use "First/ly" and "second/ly" too much.
Line 221, "same nest or nearby trees". Whats? This is the first time you mentioned how you collected the diet. Did you collect the remains? Pellets etc?
Line 245: Please explan why each stats was used (distributed normally?).
Lines 251-260: Rewrite, English
Figure 3: Percentages in the Y-axis are not clear. For example, is 80,00= 80%. Also, if A and B are a part of the same figure, I do not think you need to repeat the "before" and "after" legends.
Table 2: Needs work. Too much going on. The presentation is off.
Line 325-334: English + Not significant is not significant. Figure 4: Since none of the results are significant, can be removed without any loss of information. Instead write that There was not a relationship between diet and grassland change.
Discussion: You found breeding success increased. That is you did not find any negative effect of the loss os of grassland to the eagles. So it would help if you stuck to the discussion on what you found and not what you would of liked to find. The study's results did not show any adverse effects on the eagles. Also it is unclear how you can explain how you did not find any dietary shifts related to grassland changes (Figure 4). If this is the case, then changes in diet (fig 3) were caused by something other than changes in grasslands.
Author Response
Dear Reviewer,
Thank you for your comments. We agreed with some of the comments and didn’t accept others where we have replied and gave explanatinos.
Please, find our answers to each of your questions below:
Reviewer 2: The whole paper, especially the methods, and results, is tough to follow and needs to be rewritten due to a dire need to improve the English.
Authors response: Our manuscript has been English proofed by our native speaking colleague. He has been working with us for the majority of our publications. He has been also engaged in our most recent and already published papers in Diversity and we therefore have sent him this current manuscript and we believe he has done what was needed to English proof the text.
https://www.mdpi.com/1424-2818/14/12/1060
https://www.mdpi.com/1424-2818/14/11/1000
Reviewer 2: There is something bizarre with the font size, which varies throughout the MS. Maybe, I received the MS after a review? However, the font must be consistent throughout and follow the journal's requirements. Also, the references style did not follow the template.
Authors response: This is because of the Diversity system. We have amended this currently throughiut the text. References are done as well.
Reviewer 2: There is an overall problem with the concept of the paper. In Figure 4 shows that there were no relationships between the proportion of grassland change and the proportion of different prey change (shift). Does this mean that the changes in Figure 3 were caused by something other than grasslands? If this is the case, then is kind of undermind the title and the paper's purpose. Is the title correct? According to the data, it is not. Maybe I missed something. Also, in Figure 6: the breeding success increased after a decrease in grasslands. This also goes against the idea that habitat change is bad. The sample size is large and good, but the results do not always accompany the introduction and discussion and should be rewritten accordingly.
Authors response: We have removed Fig. 4. Nevertheless, in respect to your comment, this figure presented the relationship between the proportion of grassland and the proportion of the different prey categories seeking to find if there is any threshold in the proportion change that is clearly stated as a sub section - Threshold effect of grassland change in individual territory . This is different in general because the overall effect that is shown on Fig. 3 is clear enough and shows that both prey presence and biomass contribution significantly change. Hence, there is no need to change paper’s purpose, title, etc. In terms of the second part of your comment – the habitat change is bad because it leads to change in the diet that puts a lot of loads to the trophic system in general and leads to diverse effects on it (see lines 554-584). We agree that the Imperial eagle currently adapts well by also increasing its breeding success but different consequences can follow this adaptation that we have reviewed in detail here.
Reviewer 2: Line 13: Please add the Latin name.
Authors response: Done
Reviewer 2:
Line 18: Raptors do not forage on prey but predate, hunt, or prey on prey.
Authors response: Done
Reviewer 2:
Lines 16-23:This section is too wordy. Maybe state that prey species were eaten more and four species less the after the transformation
Authors response: This sentence presents an important findings and we didn’t remove it not to lose the information.
Reviewer 2:
Lines 24-29: If diet affects breeding, why was breeding not affected by the grassland alternation? If the goal is to determine whether grassland alteration affects the breeding and diet of the eagles, and the authors state in the title that the grassland alterations do not affect breeding, then I am not sure how these sections fit in the MS?
Authors response: Diet affects breeding, but breeding was not affected by the grassland alternation, because eagles successfully adapt by shifting grassland associated species such as European souslik and Brown hare with other grassland associated species - tortoise and hedgehog. Moreover, the Imperial eagle shifts to preying on more white storks which are not grassland dependent species. This association is analyzed in detail in the discussion section.
This section was reduced.
Reviewer 2:
Lines: 34-38: If breeding was not affected, why should grasslands be preserved? I am unsure how these recommendations fit within the results of this study.
Authors response: Grasslands should be preserved, because they are main foraging habitat for the EIE (Demerdzhiev et al. 2022). The decrease in grasslands changes the diet of the eagles while the stress in the trophic interactions is being increased as a result. By the way, all these scenarios have been discussed in detail in the manuscript
Reviewer 2:
Lines 45-48: Is this true? Are there not other natural habitats other than grassland?
Authors response: Grasslands are favorable and important for EIE.
Reviewer 2:
Lines 45- 49? I would add citations
Authors response: We added
Reviewer 2:
Line 66: What about providing new prey species? For example, agricultural pest species.
Authors response: We have never found such in the diet.
Reviewer 2:
Line 70-72: This does not make sense. Or, more likely, you provide one option only. For example, if they adapt their behavior by switching prey species, they may also increase reproduction or reproduce similarly.
Authors response: We rephrased the sentence
Reviewer 2:
Lines 82-84: Rewrite Unclear. English
Authors response: English is fluent (native speaker check)
Reviewer 2:
Lines 92- 96- Rewrite. English
Authors response: English is fluent (native speaker check)
Reviewer 2:
Lines 97-100. Unclear why this is important. Maybe move to the next paragraph
Authors response: In our opinion it is better here.
Reviewer 2:
Lines 100- 103- Rewrite. English
Authors response: English is fluent (native speaker check)
Reviewer 2:
Lines 117-120: Rewrite, English.
Authors response: English is fluent (native speaker check)
Reviewer 2:
Lines 122-138 English, kind of hard to follow/
Authors response: English is fluent (native speaker check)
Reviewer 2:
137: Study Design
Authors response: Done
Reviewer 2:
138:161: Rewite hard to understand. Also, where in Bulgaria? Size of study site? During what years? Etc et…. Missing basic information about the study site.
Authors response: We have created a map with exact coordinates, geographical names and all attributes needed to understand where in Bulgarias, what size and the periods. See Fig.1 and the relevant text in the Methods section.
Reviewer 2:
141-145: Different types of grasslands? What types?
Authors response: Check Demerdzhiev et al. (2022a) wher ewe have described all of it in great details.
Reviewer 2:
148-153: Rewrite into one sentence. Also, what about the two periods? We compared "?" (breeding and diet between two periods?
Authors response: One long sentence would be more confusing. Yes, we compare both diet and breeding between two periods.
Reviewer 2:
Lines 151-152: What habitat analysis?
Authors response: We followed the procedures described in Demerdzhiev et al. (2022a). And see the next paragraph entitled Habitat associations after the current revision.
Reviewer 2:
Line 154: What is this link? It does not work
Authors response: This is a state authority and sometimes it might not be operating.
Reviewer 2:
154-145: In both cases? What cases?
Authors response: We changed that accordingly.
Reviewer 2:
It is unclear the use of the "first step" ( line 138) and "second step" (line 168).
Authors response: We corrected these phrases.
Reviewer 2:
Lines 162-167. Why is this section not in the second step of the diet analysis?
Authors response: Done, we moved it down in the section.
Reviewer 2:
Lines 183-185: Rewrite: English
Authors response: English is fluent (native speaker check)
Reviewer 2:
Lines 185-188: Hard to follow. Isn't this written above in lines 164-166?
Authors response: It’s not, we first explain how the food niche breath has been calculated and then we explain what exactly was compared (niche breadth in the first and second period)
Reviewer 2:
189 English
Authors response: English is fluent (native speaker check)
Reviewer 2:
Line 190-191: You write above< "breeding pairs" now you use "incubating pair"
Authors response: They are equal… We considered pairs that laid eggs and started incubating as breeding pairs (Katzner et al. 2006, Demerdzhiev et al. 2015), see line 189
Reviewer 2:
Lines 191-193: Needs to be rewritten (English).
Authors response: English is fluent (native speaker check)
Reviewer 2:
206: To avoid , "Pseudoreplication"
Authors response: ok.
Reviewer 2:
Line 208: Were the eagles ringed? If not state it.
Authors response: they were not.
Reviewer 2:
Lines 208-213: English
Authors response: English is fluent (native speaker check)
Reviewer 2:
You use "First/ly" and "second/ly" too much.
Authors response: We corrected it.
Reviewer 2:
Line 221, "same nest or nearby trees". Whats? This is the first time you mentioned how you collected the diet. Did you collect the remains? Pellets etc?
Authors response: We corrected it in the revised version and clarified this matter.
Reviewer 2:
Line 245: Please explan why each stats was used (distributed normally?).
Authors response: Because part of the data were normal while the rest was not.
Reviewer 2:
Lines 251-260: Rewrite, English
Authors response: English is fluent (native speaker check)
Reviewer 2:
Figure 3: Percentages in the Y-axis are not clear. For example, is 80,00= 80%. Also, if A and B are a part of the same figure, I do not think you need to repeat the "before" and "after" legends.
Authors response: Corrected
Reviewer 2:
Table 2: Needs work. Too much going on. The presentation is off.
Authors response: But this is important information corresponding to analyses.
Reviewer 2:
Line 325-334: English + Not significant is not significant. Figure 4: Since none of the results are significant, can be removed without any loss of information. Instead write that There was not a relationship between diet and grassland change.
Authors response: We removed Fig. 4 and described this correctly in the text.
Reviewer 2:
Discussion: You found breeding success increased. That is you did not find any negative effect of the loss os of grassland to the eagles. So it would help if you stuck to the discussion on what you found and not what you would of liked to find. The study's results did not show any adverse effects on the eagles. Also it is unclear how you can explain how you did not find any dietary shifts related to grassland changes (Figure 4). If this is the case, then changes in diet (fig 3) were caused by something other than changes in grasslands.
Authors response: See above our explanations accordingly.
