Stable Isotope Analysis Supports Omnivory in Bank Voles in Apple Orchards
, Vitalijus Stirkė 1, Andrius Garbaras 2, Raminta Skipitytė 2 and Laima Balčiauskienė 1
Round 1
Reviewer 1 Report
The manuscript by Linas Balčiauskas et al. is devoted to determining the analysis of the bank vole (Clethrionomys glareolus) feeding strategy in apple orchards using stable isotope analysis of fur. The topic undoubtedly fits both in the Agronomy journal and in the Section 'Ecosystem, Environment and Climate Change in Agriculture'. However, the manuscript only marginally fits into the topic of the Special Issue (Biodiversity in Fruit Orchards); it more belongs, for example, to the realm of food ecology.
As far as I can judge as a non-native speaker, the work is comprehensibly written and innovative on several aspects, esp. the methodology (tracking stable isotopes). Small mammals in orchards have been rather overlooked in research so far, despite they can play a fundamental role for target tree species (especially bark-damaging rodents, such as Microtus spp., Arvicola spp. etc.). Similarly, only marginal attention has been paid to the bank vole outside the forest environment. That's why basically every new knowledge from these areas is very valuable.
I have a few suggestions that I believe could improve the resulting article. They are listed chronologically, resp. in the order in which they appear in the text.
L23 and 440 – I was interested in the described 'ecological plasticity' of the bank vole. The same findings have been yielded by comparison of the content of nitrogenous substances in the stomach contents of this species (the widest ecological niche of the observed rodents). Unlike the other observed species of small mammals, the bank vole showed significant changes in the content of nitrogenous substances in the food depending on the year and habitat (for a comparison, see Cepelka et al., 2014). That comparison demonstrates the exceptionality of the bank vole species and suggests possible topics for further research.
L63-66 – For a broader context, in addition to the mentioned classic analyses of the consumed food and the composition of the GIT, I think it would be appropriate to also mention the analyses of the nutrient content in food (e.g., Butet, 1996; Palo and Olsson, 2009; Cepelka et al., 2014).
L226 – In Figure 2, some colours are hard to distinguish. It would be more appropriate to use different shades, or even better, different hatching.
L242 and L244 – redundant 'per'
L405-406 – living vertebrates (frogs and bird nestlings) in the list need to be explained. The link provided does not mention neither bird nestlings nor frogs, and I am not aware that the bank vole consumes them either. Their cadavers are different case. Please clarify the text or add a citation proving the consumption of living vertebrates by the bank vole.
L431 – in agricultural systems, I perceive a sudden change in food availability (due to a one-time harvest or application of fertilizer or pesticide) as a more fundamental limit for rodents than the amount of food.
The extent of changes fit the criteria of a minor revision.
The references used:
Butet, A. Does food quality Drive Cycle in Microtus arvalis? Study on a French Atlantic Marsh Population. Proc. I Eur. Congr. Mammal. 1996, 177–188.
Palo, R.T.; Olsson, G.E. Nitrogen and Carbon Concentrations in the Stomach Content of Bank Voles (Myodes glareolus). Does Food Quality Determine Abundance? Open Ecol. J. 2009, 2, 86–90, doi:10.2174/1874213000902010086.
Čepelka, L.; Heroldová, M.; Jánová, E.; Suchomel, J. The Dynamics of Nitrogenous Substances in Rodent Diet in a Forest Environment. Mammalia 2014, 78, 327–333, doi:https://doi.org/10.1515/mammalia-2013-0017.
Author Response
Dear Reviewer,
answers to ypur comments attached
Author Response File: 
Author Response.pdf
Reviewer 2 Report
This paper assesses the trophic niche of C. glareolus. The aim of the manuscript is however not well defined. The title focuses on the trophic niche, but much of the paper is about capture results. You need to decide first which is the focus of your paper and then build it around. I have the impression that the trapping results are already published in several papers, so I do not see why this is important in the trophic niche context. The hypotheses also appear somewhat artificial. Of course would you expect a species to occupy a separate trophic space than the other species living in the same area. However, you did not study all species but just a few others that you expected/knew to be herbivores, insectivores or granivores. I therefore think you should refocus the paper on trophic niches. My second concern is with the potential food items. In Figure 5, it seems that the diet of C. glarelus is not somewhere amid the potential food items but outside. How can you explain this? Maybe you missed out important food items? This would need to be addressed. Another concern is about the presentation of the manuscript. In my opinion, you repeat too often results in text, tables and figures. You just need to present it once, best in a figure or table, and then comment on it in the text. The language needs more editing by a native speaker. Sometimes the choice of terms is unclear or seems not to make sense, such as “complex communities”, “synchronous responses”, “fragmentary study”, “differences were not expressed”, “best represented”, “small mammal trophic groups”, “crown closure (maybe you mean canopy?)”, “isotopic niches”. Some sentences are also not clear (e.g., lines 42-44). You should also avoid using the passive voice, especially when you write about something you did. I therefore think you should refocus the paper, shorten it to the essentials and add, if possible, more potential food items to the analyses.
Some detailed comments:
Line 96/97. Forest ecotone is not the right term. An ecotone is a transition zone so it must consist of two habitats, in your case probably a meadow-forest ecotone.
Line 147-148. If you repeated samples, so why don’t you report the results here (it belongs to the methods not the results section in case you reported them later)?
Line 158 and later. CI is more informative than SE, so it is enough to report this.
Line 173-174. Setting confidence levels here is useless, better provide the exact p value and the reader can judge.
Line 196-205. Not really results, fits better in method section.
Table 2. you should provide information about the habitat instead of “control” throughout the manuscript. What is the point of this table?
Lines 211-250. Why is this important to the aim of the paper?
Lines 252-282. To much repetition of results presented already in figures. You should not repeat results in the text, only point to the important things.
Figure 3. SE is no interval, you should replace it with CI here and elsewhere. Not clear which other species are behind the granivores, herbivores and insectivores. A better way to present data would be to individually show species here and mark if they are granivores, herbivores, or insectivores.
Lines 297-303. Again, to much repetition of results, the table is sufficient.
Fig5. Change SE to CI here, then you can directly see which values differ from each other. The value for C. glareolus is clearly different from the tested diet items. So obviously they eat some food that you did not test. Table 3 seems to be a repetition of results also (better) presented in Fig5, so table 3 should be deleted.
Table 4. Most of these correlations are not significant, suggesting that the significant correlations might just be pseudo-correlations. Maybe there is a better way presenting these results?
Table 5. Colony 1-3 are no habitats, please provide here the actual habitats, otherwise this info is of little use here. SE needs to be changed to CI, then all averages can be directly compared. There is no reason just comparing all values to the apple orchards, so you can anyways delete the test.
Author Response
Dear Reviewer,
answers to your comments attached
Author Response File: Author Response.pdf
Reviewer 3 Report
This is a very interesting paper that tests omnivory in bank voles from a small mammal community living in a commercial apple orchard in Lithuania. The authors used stable isotope analysis to identify the levels of omnivory, as well as differences related to body mass and gender. The paper is well designed, and the data are important and have been analyzed properly and thoroughly. There are some flaws, mainly in the discussion section (please see comments below). The language also requires a few edits and caution in some parts to assure that the text flows well.
Although the introduction is relatively well developed, in some places it seems as it presents disparate data that do not flow very well and seem not to support the predictions at the end of this section.
Lines 85-88: Related to this, usually the smaller the mass the higher the energy requirements and thus a shift to animal food matter (e.g. the case of soricids). Thus prediction 2 seems a bit awkward. Can the authors provide evidence to support their prediction? (this may be one of the reasons that it was not verified).
Lines 110-115: snap traps? Isn’t here a question of ethics, as many animals had to be sacrificed for the purposes of this study?
In the methods section the authors do not present on what grounds they classified the studied animals in the different trophic classes (insectivorous, granivorous, herbivorous, omnivorous). They only present their data in the first paragraph of the results section in an ad hoc manner. Were they based on the literature? And if yes, which proportions for each food class were considered as threshold to classify each species to each category. This is not clear and needs to be amended.
The results are very well presented and have been analyzed thoroughly to test the predictions forwarded in the introduction. They are clearly displayed in graphs that support the omnivory of the species and test for habitat, condition, size and gender differences. However, the discussion falls short to exploit in a concise and integral way the rich material of the results. The discussion seems more of a conglomeration of separate paragraphs that do not appear to flow to a certain way. What do the authors need to support and, thus, discuss in detail in this paper? Omnivory and its potential variation is the key finding of this research but their results can go further and clearly support the trophic plasticity of the species depending on the environmental conditions tested. I think that the authors need to focus more carefully on this.
Author Response
Dear Reviewer,
answers to your comments attached
Author Response File: Author Response.pdf
Round 2
Reviewer 2 Report
The revision clarified the manuscript a little, but the presentation has not much improved. In my opinion, there is too much repetition of results in the text. The manuscript would profit from shortening and structuring it better. Some terms are still not well used. For example, “fitness” usually describes the reproductive success of an individual, it is not a good term for the relation of body mass to length, you could use “body mass index” here or something similar. I will not repeat my propositions of the first review, at the end it is the responsibility of the authors to present the results in the best way possible and the decision of the editor if the quality of the manuscript is sufficient for publication. I however strongly recommend to reconsider my comments from the first review and thoroughly edit the manuscript.
Author Response
Comments and answers, Rev#2 round 2
Nevertheless, there are a few things that still need to be amended and are presented below (mainly minor):
- 37. According to their teeth …
Answer: comma removed
- 55. I would suggest that the authors use Myodes glareolus throughout the paper, as this is the currently recognized name of the species (https://www.iucnredlist.org/species/4973/197520967)
Rebuttal: we cannot agree with that, as IUCN is not the source for taxonomy. Currently species is again C. glareolus, and we provide necessary reference. In our previous papers we were criticised for using Myodes glareolus.
- 90. …(1) to demonstrate that C. Glareolus ….
Answer: changed as requested
- 95-97. Still the authors need to explain what they expect in terms of mass differences, e.g., higher in smaller or more fit ones? Regarding sex differences, the authors clearly expect females to demonstrate higher rates of N values because of pregnancy and lactation demands, but what about body mass or fitness differences??? Please clarify.
Answer: we would not like to say that. Please see change „(2) concerning intraspecific patterns of diet, we tested whether higher nitrogen values were characteristic to females with forming embryos or in lactation and/or differ in individuals with different body mass/individual fitness.“ Now it should be clear, that we do not say higher or lower, just different.
- 140-141. …groups according to [21-24….
Answer: word „trophic“ removed as suggested
- 358. Our main goal was to demonstrate C. Glareolus ….
Answer: changed as requested
- 367-368. …and even preferring them…
Answer: changed as requested
- 418. …from floods or fertilizers.
Answer: changed as requested
- 433. …a granivorous small mammal …
Answer: changed as requested
- 447. …are very close to human settlements [19]….
Answer: changed as requested
- 457. …is one of such traits, enabling …..
Answer: changed as requested
Reviewer 3 Report
The revised version of the manuscript is clearer, flows better and more concisely and the authors have adequately replied to the suggested comments. The discussion now flows very well, and arguments follow a logical order to help the reader understand the importance of omnivory in voles.
Nevertheless, there are a few things that still need to be amended and are presented below (mainly minor).
l. 37. According to their teeth …
l. 55. I would suggest that the authors use Myodes glareolus throughout the paper, as this is the currently recognized name of the species (https://www.iucnredlist.org/species/4973/197520967)
l. 90. …(1) to demonstrate that C. glareolus ….
l. 95-97. Still the authors need to explain what they expect in terms of mass differences, e.g., higher in smaller or more fit ones? Regarding sex differences, the authors clearly expect females to demonstrate higher rates of N values because of pregnancy and lactation demands, but what about body mass or fitness differences??? Please clarify.
l. 140-141. …groups according to [21-24….
l. 358. Our main goal was to demonstrate C. glareolus ….
l. 367-368. …and even preferring them…
l. 418. …from floods or fertilizers.
l. 433. …a granivorous small mammal …
l. 447. …are very close to human settlements [19]….
l. 457. …is one of such traits, enabling …..
Author Response
Comments and answers Rev#3 round2
Comments and Suggestions for Authors
The revision clarified the manuscript a little, but the presentation has not much improved. In my opinion, there is too much repetition of results in the text. The manuscript would profit from shortening and structuring it better.
Answer:
Line 222: we additionally deleted „from 0 in site 7 to 44.6% (CI = 32.4–57.6%) in site 9 and 42.8% (CI = 35.6–50.2%) in site 6“
Line 291: we additionally deleted (−25.41‰)
Line 310-311: we additionally deleted δ15N = –12.41‰, and e, δ15N = 5.38‰,
There are no more values/numbers, repeated in the text. Other numbers are averages, not presented in the other form, or statistical tests, which we would not like to delete.
Comment: Some terms are still not well used. For example, “fitness” usually describes the reproductive success of an individual, it is not a good term for the relation of body mass to length, you could use “body mass index” here or something similar.
Answer: fitness was changed to „body condition index“ across the text. We stay on this according Moors (1985), as it was used by many previous publications, and to avoid mismatch to BMI in himan, used to describe obesity.
Comment: I will not repeat my propositions of the first review, at the end it is the responsibility of the authors to present the results in the best way possible and the decision of the editor if the quality of the manuscript is sufficient for publication. I however strongly recommend to reconsider my comments from the first review and thoroughly edit the manuscript.
Answer: It is not easy to answer general comment, such as “not the best way”. In the first answer we presented our framework for discussion. Reshaping of the text in discussion was also done. Two other reviewers had no objections as for the text flow, therefore we are not introducing further changes.
