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After reviewing this revised version of your manuscript, I see that the main comments suggested by the reviewers have been included, while the suggestions not considered are justified in detail. Therefore, I am satisfied with the current version and consider it ready for publication.
[# PeerJ Staff Note - this decision was reviewed and approved by Dezene Huber, a PeerJ Section Editor covering this Section #]
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The authors have addressed all reviewer comments thoroughly and satisfactorily. I have no further objections or suggestions regarding the revised manuscript. I am therefore pleased to recommend it for publication in PeerJ. My compliments to the authors for presenting a clear, well-structured, and insightful study on individual specialization.
Thank you very much for your manuscript titled “Individual and population variation in isotopic niche between two sympatric cormorant species” that you sent to PeerJ.
This study presents very valuable and relevant information on seasonal changes in individual and population niches of two sympatric cormorant species in Chile.
As you will see below, comments from referee 3 suggest a minor revision while reviewers 1 and 2 suggest a major revision before your paper can be published. Given this, I would like to see a major revision dealing with the comments. Their comments should provide a clear idea for you to review, hopefully improving the clarity and rigor of the presentation of your work. I will be happy to accept your article pending further revisions, detailed by the referees.
Reviewer 1 suggests improving various points throughout the document, especially within the methodology.
Reviewer 2 suggests a more detailed explanation of the concepts and examples that support the study hypotheses, which could be supported with a figure. He also suggests editing figures and tables and strengthening the presentation of results.
Reviewer 3 suggests more specificity on points such as the study's predictions, covariance matrices, and indices used. They also suggest improving the discussion.
Please note that we consider these revisions to be important and your revised manuscript will likely need to be revised again.
**PeerJ Staff Note:** Please ensure that all review, editorial, and staff comments are addressed in a response letter and that any edits or clarifications mentioned in the letter are also inserted into the revised manuscript where appropriate.
1. BASIC REPORTING
Line 13: Is it a journal policy to divide the abstract in subheadings? Not what I would personally do, but strictly spoken not wrong either
Line 23: while not strictly required, I would add the English/common name of these species as well, especially in the abstract.
Line 28: is IS (individual specialisation) the same as WIC? If possible, I would shortly integrate this in abstract, because now it is not clear how this was determined/how this relates to WIC/BIC/TNW.
Line 52-56: But niche partitioning (and individual specialisation) can also be affected by sex and size (and age). E.g. for cormorants species where males and females exploit different areas (e.g. https://journals.biologists.com/bio/article/13/5/bio060336/347525). Size and sex can affect which resources can be reached by a specific individual (and therefore shape individual niche/specialisation). Age might also affect/reflect the experience/capacity of an individual to exploit specific resources. So I don’t think it is valid to say size, sex and age do not play a role.
Line 59: “specialist species”: I assume here you mean species with a specialisation on the species level? This sentence is a bit confusing.
Line 60: “diets overlap”: overlap with what? Intraspecific or interspecific?
Line 80-84: I think it would be good to add partial migration here, especially when considering cormorants. If you consider this within dispersion, this is fine, but then maybe still mention it.
Line 94-100: you state that dispersive species reduce specialisation during breeding, which is maybe true for the species you mention, but especially for cormorants there is quite some evidence of individuals showing high specialisation during the breeding season, even if they disperse/migrate afterwards (e.g. https://link.springer.com/article/10.1007/s00227-024-04541-z, https://onlinelibrary.wiley.com/doi/full/10.1111/ibi.13371)
Line 109-110: “niche overlap”: intraspecific or interspecific? It would probably be good to go through your manuscript and check throughout for mentions of things like “niche overlap” and “specialisation” if it is interspecific or intraspecific. This is not always clear from the context, and adding “interspecific” or “intraspecific” in some place might make this easier on the reader (especially as this manuscript talks about both).
Line 144: It would be good to give a rough estimate of colony sizes for the cormorants. I appreciate that literature supported estimates might not be available, but for the reader it would be good to have an idea if we are talking about 10's 100's or 1000's of individuals.
Line 147-149: It would be good to add the English/common names of these cormorant species as well.
Line 201-201: For some reason this sentence makes it sound like all samples were mixed.
Line 338: I don't think this section needs a subtitle, and in any case "sampling success" sounds a bit odd
Line 392: As mentioned in another comment, to me it is quite confusing why this aspect was added, and it is not really integrated in the discussion.
Line 407: I would suggest to quickly reiterate the goals of the paper in the first part of the discussion.
Line 408: Right now there is little structure in the discussion, which makes it hard to follow in places. Adding some subheadings would likely help to improve clarity. if I recall correctly, m1 and m2, and m3 and m4 belong together. Why not use these as subsections (m1 and 2 (competitive exclusion); m3 and 4 (optimal foraging theory)). Now the structure of the discussion is quite hard to follow.
Line 419: here you could do a subheading "competitive exclusion" (or similar)
Line 419: “M1, segregation of population niches,” instead of just M1? Then you could do this throughout discussion so reader avoids scrolling back and forth (as you cannot expect anyone quickly reading your paper to remember what M1, M2,… stand for.
Line 423: “Unexpected finding”: is it though? if there is enough food (to population size), competition is not necessarily limiting. I would maybe not call it unexpected if you then have a completely reasonable explanation in the second part of the sentence.
Line 458-461: But after dispersing, cormorants can also show central place foraging, just in areas with other opportunities/less competition. (e.g. https://link.springer.com/article/10.1007/s00227-024-04541-z)
Line 463: Here would be a good place to add a new subheading (“optimal foraging”).
Line 472-475: But also, it is dispersive, so they might feed on something else during the nonbreeding period because some individuals are in totally different locations (with different food availability).
Line 517: As a note to the authors: Isotopic mixing models sound nice in theory, but unless you have captive animals to obtain e.g. species and resource specific discrimination factors, applying them to wild animals is very hard/impossible and might cost a lot of time and effort for little extra results.
Line 518: metabarcoding cloacal swabs might also be a promising technique here for dietary sampling.
Figure 1 and Figure 2: For both it would be good to add some raw data points, this is generally more informative.
Line 188: “prevent repeated measures”: wouldn't that have been of interest? Especially if you can capture an animal both during the breeding season and non-breeding period.
Line 194-195: How many primaries and how many body feathers were collected?
Line 197-198: any reference for these feathers being moulted at that time (i.e. primaries during breeding and body feathers during non-breeding)? This is a very important assumption of your manuscript.
Line 213-217: I assume you used plasma, red blood cells, primaries and body feathers as "repeated measures" to obtain WIC. However, did you apply any discrimination factors to account for expected differences between tissues? While I understand that species specific discrimination factors might not be available, you could use a general one to correct feathers and blood to the same "level". If no correction is applied, the combination of feathers and blood to calculate WIC will automatically lead to an overestimation.
Line 243: Did you have any regurgitates from cormorants you caught? if so, these would have been interesting to include (or if you repeat the study in the future, would be worthwhile to keep them)
Line 263: This is a bit of a confusing section, especially as you bring in other groups of species here ( which is not really in the introduction). Additionally, I am not sure how much this section really contributes to the paper, I appreciate a lot of work has gone into it, but I am really questioning how much it contributes to the overall results. The reason I am questioning the inclusion is that this aspect of the paper is not really introduced as a goal, but takes up a lot of the methodology section. Subsequently, in the results, it has only a limited mention, and in the discussion I cannot clearly find where this section comes into play. It might be associated to one of the mechanisms you are testing, but in this case this is not really clear and should be emphasized more.
Line 272-273: You are bringing in some other groups of birds, but how much do these compete with cormorants for the same prey? If your cormorants have a strong pelagic prey component, I would expect some competition, but if not, I would expect for cormorants to predominantly target benthic prey, opposed to pelagic prey for the other species.
Line 309: While I think the statistical analysis section is complete, it is quite confusing throughout and it is not always clear what is tested with any specific analysis. I think just adding in some places e.g. “to test M1”, “to test M2”,.... would clarify a lot. Currently I am getting lost. It also seems the order in which analyses are mentioned is not entirely consistent with the order things are introduced in methods, presented in results, which makes it extra confusing. I am sorry, but after going through this section a couple of times I am still not sure which specific analyses contribute to which goal/which result.
Line 345: Where these isotopic values corrected for discrimination factors, because else this pattern is just what would be expected (e.g. feathers enriched compared to blood) (and you will also need to correct to compare these samples as being representative for isotopic niche at different times). Even when discrimination factors for this species are likely not available, you could use values from another cormorant species as a proxy (or other birds as e.g. plasma-RBC might be hard to get for cormorants).
Line 356: I am confused which sample was used where to get your niche components. E.g if you catch a bird during the NB period, you have three samples for NB period (RBC, plasma, body feather) and one for B period (primary), if you catch a bird during the breeding period, you have primary, RBC and plasma for this period, but only body feather for the NB period. Did you split samples somehow to account for this, were different individuals used to be representative for NB and B period? This should be clarified in the methods.
Line 358 onwards: Which tests were used to obtain these P values, this is really not clear from the statistical analyses section of your methodology.
Line 278-284: Is this data available anywhere? I could not find it in the supplementary tables or in the repository. So please verify if and where this is available.
In general, I think this is an interesting manuscript contributing interesting findings to the underlying mechanisms of niche separation. The authors also used an interesting study system by looking at the overlap in niche of two sympatric cormorant species at different parts of the annual cycle. However, while some sections are very well written (introduction, most of the methods, most of the results and the majority of the discussion), some sections of the methodology are not entirely clear or a bit vague and will need further clarification to bring the quality of this manuscript up to the required standards.
This is an insightful and overall well-written article that clearly addresses the mechanisms behind the coexistence of two sympatric species, examining both inter- and intraspecific segregation across different study levels (individual and population).
Given the complexity of the topic—due to its involvement with multiple study levels and contrasting hypotheses—it would be beneficial to provide more context on the theoretical background. Specifically, a deeper explanation of the various concepts would be helpful, particularly when contrasting population-level and individual-level partitioning. It would also enhance the reader’s understanding to introduce examples or references for the four hypotheses being tested. This additional information would better equip the reader to follow the four hypotheses presented later in the paper.
Moreover, a schematic figure illustrating the four tested mechanisms (M1-M4) would be valuable for visualizing the concepts and further aiding comprehension.
The overall structure of the article is well-organized. However, there are a few areas that need attention for greater clarity and transparency. Specifically, the tables and figures lack the sample sizes (N) for each variable, which should be included for completeness.
Additionally, instead of presenting M1 results in a table format, it would be more beneficial for the reader to have a figure that visually represents these results (as mentioned in the general comments). This would provide a clearer, more intuitive understanding of the data concerning population niche overlap.
While raw data are not available in the current manuscript, it would be useful to provide a file containing either the raw or processed data used to calculate the indicators of ecological opportunity and competition. Presenting intermediate steps in the results section before the final indicator values would also improve transparency—alternatively, these details could be included in a supplementary file. For instance, listing the prey species found in the pellets, along with their frequency of occurrence or abundance per season, would give readers more insight into the data behind the indicators. Similarly, for the competition indicator, raw count data or a table summarizing the count results should be made available for reference.
Research question is well defined, relevant & meaningful. Overall complies with rigorous investigation performed to a high technical & ethical standard, although some details need to be stated concerning handling time of the cormorants during breeding season (see comment in the pdf).
Overall, the methods described with sufficient detail & information to replicate; some comments need to be addressed (see comments in the pdf).
Most underlying data have been provided; they are robust, statistically sound, & controlled. As mentioned previously, some extra information is required concerning number of samples (N) presentation, raw data and improvement of M1 results presentation (see basic reporting and comments in the pdf). The conclusions are appropriately stated and connected to the original question investigated.
This is a very interesting and overall well-written paper in which the authors aim to unravel the mechanisms behind the coexistence of two sympatric species, addressing both inter- and intraspecific segregation across different levels of study (individual and population). The study is particularly impressive, given the large number of samples collected from species and study sites that are often challenging to study. The use of night captures and repeated sampling of the same individuals over time adds significant depth to the research. Congratulations to the authors for this tremendous and commendable effort!
The main issue to address concerns the M1 hypothesis: “Segregation of population niches , either through contraction or shift in niche position to enhance partitioning of resources between species.” The current analysis—comparing mean C and N isotopic values between species, and isotopic niche width overlap—does not clearly demonstrate whether isotopic niches overlap in space. A proper assessment requires a bivariate analysis that examines both niche position and overlap, such as using Bayesian Standard Ellipse Areas (SEAB) with the SIBER package. I also recommend including a bivariate C–N plot showing niche position (not just niche width), if feasible given the dataset. At present, the manuscript appears to conflate overlap in niche width with overlap in isotopic niche, which are distinct concepts, and should be used together to address M1. This distinction must be made explicit throughout the text, and isotopic niche overlap should be analysed and reported separately. Not only would this approach be more accurate, but it would also allow direct comparison with other studies.
As mentioned above and throughout the PDF, the introduction and methodology require more detail (see specific comments in the file). At times, the text is difficult to follow, as if the manuscript had been condensed to the point where essential background or methodological information is missing—particularly for readers unfamiliar with individual specialization and TWN calculations. Below, I provide some suggestions, which are also detailed in the in-text comments.
- Introduction: I suggest further background details on population and individual segregation; introducing examples or references for the four hypotheses being tested; I suggest adding a schematic figure illustrating the four tested mechanisms (M1-M4)
- Methods and results: it is not clear which tissues have been used for each combination of species/period, and for the calculation of the different values (ej. BIC-WIC). As far as I understand, different isotopic data from different tissues reflecting different period of time and integration period were used to calculate BIC-WIC for each individual. This should be clarified (methods and table 1). And when comparing values issued from different tissues, it should be stated and discussed as to how this could affect the results and the comparison, and/or if you think it doesn’t hinder comparison because of data transformation it should also be stated.
- Results: Tables, figures, and reported results lack sample sizes (N) for each variable. These should be included to allow proper interpretation and comparison of the findings.
- Intermediate steps and data needed to understand results of indicators of ecological opportunity and competition.
- Discussion: Several points require further elaboration (see detailed comments in the PDF). Expanding these sections will strengthen the interpretation and contextualization of the results.
I commend the authors for compiling an extensive dataset through detailed fieldwork across multiple seasons. The manuscript is also clearly written in professional, unambiguous language. Addressing the points outlined above will further strengthen the work and bring it closer to acceptance.
General comments:
The manuscript is well written. The authors have been concise, clear, and coherent in their writing, and the article reads smoothly.
The study addresses intrapopulation trophic variation in two sympatric seabird species during different reproductive periods. Specifically, it examines how total niche width and individual specialization vary between breeding and non-breeding periods in species with different dispersal strategies (resident vs. dispersive). The authors analyzed stable isotope data from 111 individuals (with repeated measures) to calculate niche components (TNW, BIC, WIC) using classical mixed models. While the introduction is well written, the authors should be more specific in their predictions, grounding them in the cited literature and the characteristics of their study system. The methodology is robust, although it is still necessary to clarify the type of model used to estimate the (co)variance matrices. Additionally, the relative contribution of intra- and interspecific competition to the index used should be made clear. The results are clear and comprehensive, supported by simple yet elegant figures. I suggest a few modifications to improve the figures. An interesting strength of the article is the authors’ effort to articulate the potential mechanisms driving patterns of niche variation and individual specialization (IS) between populations. However, the discussion could be strengthened by presenting the classic mechanisms in a clearer and more structured way. As it stands, it is somewhat diffuse, which may leave the reader uncertain about which mechanisms are likely to carry more relative weight (e.g., ecological opportunity, competition, species-specific biological idiosyncrasies).
Overall, the manuscript is well presented and requires only minor changes. Its originality and impact would be enhanced if the findings were integrated and interpreted more consistently in light of classical references already cited in the introduction and discussion (e.g., Araújo et al., 2011; Van Valen, 1965).
Specific comments:
L52: Please define individual specialization (IS) sensu Bolnick (2003) before discussing its eco-evolutionary consequences.
L53: Which ones? Please cite specific examples.
L88: In this paragraph, two classic causes of individual specialization (ecological opportunity and competition) are mentioned, but the authors do not cite seminal works on the subject, such as Araújo et al. (2011). I recommend better articulating the causes of IS with the study-species biology. This would help the reader understand the hypotheses and the results presented.
L118: Authors used repeated stable isotope measurements per individual (multi-tissue approach), which allows the calculation of individual specialization. Without repeated measures, WIC could not be estimated - At least, not with the models suggested by Ingram et al. 2018. I suggest emphasizing this information in this paragraph and in the abstract, as well as highlighting its importance in the methodology.
The authors present the objective of the stud, the main hypotheses and predictions clearly and objectively, with appropriate references supporting the information provided. However, authors could be more specific and better highlight an interesting research gap in individual specialization and diet studies that is not entirely clear in their study: the investigation of the mechanisms that drive population niche variation and individual specialization. Although the existence of IS is well documented, empirical evidence on which mechanisms are most important in promoting IS remains limited. Emphasizing this point could enrich the manuscript and clearly present to readers a research gap that the study could help address.
Specific comments:
L126: The theoretical framework used to support the hypotheses seems appropriate and well chosen. However, which mechanisms are more likely to be at play? There appears to be some evidence suggesting that certain outcomes may be more probable than others. I suggest the authors clarify this and present the hypotheses in a more structured way. For example, mechanisms M1 and M2 could potentially be articulated together: if individuals reduce their individual niche, this would lower WIC (M2), which increases individual specialization, but at the same time, the overall niche would contract (M1).
L197: Where do these temporal estimates based on feather type come from? Please provide supporting information or references, if available.
L201: It is very important and helpful for interpreting the results to know the time period each tissue type integrates. I suggest briefly clarifying this information for each tissue.
L222: This is correct. However, the most intuitive formulation of this metric was proposed by Bolnick et al. (2007), using the V index: 1 – IS. I believe it is worth acknowledging the original source of this approach.
L226: I follow and understand the analysis and how BIC, WIC, and TNW were obtained. However, it is not clear how the models were run. Were these two-dimensional mixed models? Multidimensional models? Some studies have used one-dimensional models, others two-dimensional, and others multidimensional models. Therefore, it is important to clarify this information, as results in IS can sometimes differ substantially depending on the model used. Please provide a clearer justification for the use of these models.
L295: At this point, I assume that the index used in Figure 3 places greater emphasis on interspecific competition. What exactly does it represent? Does it encompass all competitive interactions (both intra- and interspecific), or is it focused on one type of competition? I believe this clarification is important for interpreting your results, as inter- and intraspecific competition are different drivers and may have distinct effects on the degree of individual specialization.
L300: Did you construct the phylogeny? How was this phylogeny constructed or obtained? Ecological analyses that include a phylogenetic component generally require a consensus phylogeny (e.g. Frackleton et al. 2002; AmNat). Therefore, the authors could include more information about the source and method used to obtain the phylogeny.
L334: The core size of ellipses is important and should be cited here. The size of the ellipse directly affects the overlap between species. Are these metrics similar to SEAb or SEAc (sensu Jackson et al. 2002)? Please clarify whether this approach uses a Bayesian framework and what type of ellipse was employed
General comments:
The methodology and techniques used by the authors are robust and well-known. Although some of the models require further explanation in greater detail (see comments above in Section 2), the methods employed are appropriate and reproducible.
Specific comments:
L343: Improve the ESM. the table name, title description, and authors of the ESM are missing.
L358: What statistic does 0.999 represent?
L399: During the breeding season, interspecific competition increases greatly in both species (L. 399; Results in Abstract). However, in one species the IS decreases while in the other it increases. How do the authors explain these results? Please discuss this point. Following the classical hypothesis (again, Araújo et al. 2011), there are clear predictions about the effect of interspecific competition on IS.
L503: I understand it is important to acknowledge the limitations of SIA, but I don’t think they justify the results obtained. If you prefer, some limitations can be mentioned in the Introduction or Methods section, but cautiously, so as not to imply that these caveats prevent interpretation of the results. Stable isotopes have methodological limitations, but it is a widely accepted technique in trophic and isotopic ecology, with countless evidences supporting its consistency and robustness.
L521: In line with the previous comment, this paragraph would be more suitably placed in the Methods section rather than in the Discussion.
Figures 1 and 2
- I strongly recommend the authors include individual data points in the plots. This is important because, in a study at the individual-population level, being able to visualize where individual C and N values fall in isotopic space is essential. Furthermore, depicting individual niches would help in understanding the IS values obtained (a higher IS value indicates greater interindividual niche differentiation).
- I recommend that the authors include the parameters of the ellipses presented in the legend; if these are Bayesian ellipses, please specify the isotopic niche area they represent (e.g., 95% credible interval ellipses).
- How have the C and N axes been scaled? Please explain this in the figure legend.
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