Downtown diet: a global meta-analysis of increased urbanization on the diets of vertebrate predators

Predation is a fundamental ecological process that shapes communities and drives evolutionary dynamics. As the world rapidly urbanizes, it is critical to understand how human perturbations alter predation and meat consumption across taxa. We conducted a meta-analysis to quantify the effects of urban environments on three components of trophic ecology in predators: dietary species richness, dietary evenness and stable isotopic ratios (IRs) (δ13C and δ15N IR). We evaluated whether the intensity of anthropogenic pressure, using the human footprint index (HFI), explained variation in effect sizes of dietary attributes using a meta-regression. We calculated Hedges’ g effect sizes from 44 studies including 11 986 samples across 40 predatory species in 39 cities globally. The direction and magnitude of effect sizes varied among predator taxa with reptilian diets exhibiting the most sensitivity to urbanization. Effect sizes revealed that predators in cities had comparable diet richness, evenness and nitrogen ratios, though carbon IRs were more enriched in cities. We found that neither the 1993 nor 2009 HFI editions explained effect size variation. Our study provides, to our knowledge, the first assessment of how urbanization has perturbed predator–prey interactions for multiple taxa at a global scale. We conclude that the functional role of predators is conserved in cities and urbanization does not inherently relax predation, despite diets broadening to include anthropogenic food sources such as sugar, wheat and corn.

I am writing to inform you that your manuscript RSPB-2021-1205 entitled "Downtown Diet: a global meta-analysis of urbanization on consumption patterns of vertebrate predators" has, in its current form, been rejected for publication in Proceedings B.
This action has been taken on the advice of referees, who have recommended that substantial revisions are necessary. With this in mind we would be happy to consider a resubmission, provided the comments of the referees are fully addressed. However please note that this is not a provisional acceptance.
The resubmission will be treated as a new manuscript. However, we will approach the same reviewers if they are available and it is deemed appropriate to do so by the Editor. Please note that resubmissions must be submitted within six months of the date of this email. In exceptional circumstances, extensions may be possible if agreed with the Editorial Office. Manuscripts submitted after this date will be automatically rejected.
Please find below the comments made by the referees, not including confidential reports to the Editor, which I hope you will find useful. If you do choose to resubmit your manuscript, please upload the following: 1) A 'response to referees' document including details of how you have responded to the comments, and the adjustments you have made.
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Sincerely, Professor Gary Carvalho mailto: proceedingsb@royalsociety.org Editor comments to Author: Thank you for your resubmission of the above manuscript. You will see that we have received three responses from referees, and that two out of the three are happy with the proposed revisions made. I continue to have two major concerns, the first relating to comments concerning the overall design and analysis of data, and the second an apparent lack of response to my specific editorial questions.
1. An original reviewer, referee# 1, continues to question a fundamental issue relating to the comparisons being made, and the validity thereof. I have also looked at the manuscript myself, and while there remains a disparity of opinions, I find the case made relating to the classification of urban information, not fully convincing. I agree, and clearly the issue raised relating to sample sizes is fundamental, and I also am unable to find these details in your manuscript. I very much appreciate the additional detail you have provided concerning the available data that you have, but there does need to be a high level of transparency, that is readily accessible, concerning the robustness of the comparisons made. It is indeed very unusual to request a second major resubmission, but I continue to see significant potential and likely impact of your work. I have classified it as a resubmission, since clearly, in terms of the inferences, and likely impact, we do need absolute confidence that despite the shortcomings, that inferences made are indeed sufficiently valid to avoid bias and any misunderstandings.
2. Below (between the margins added), I repeat part of my original editorial letter, concerning the formatting and content of evidence synthesis manuscripts, with reference to specific elements: in your response letter, and forgive me if I have somehow missed any detail, I cannot find the specific and explicit responses to the issues I raised. While of course I reviewed the manuscript more fully, I do need to know the extent to which each of these issues have been fully considered and addressed. I duplicate part of the original letter below: Crucially, as you will be aware, for an evidence synthesis manuscripts, it is vitally important that the methodology is sufficiently transparent and accessible to provide the readership with confidence in any inferences drawn. While there are of course many definitions of meta-analyses, essentially the analytical approach summarizes the results of several studies, allowing researchers and policymakers to understand both the average effect across studies and its variability, thus leading to more informed decisions about important policy issues. Currently, the methodology is not sufficiently informative, and inclusion of a clear protocol is critical given the complexity of the steps involved, and the fact that variance in even small decisions could influence the validity of the results. A coherent and informtaive published protocol facilitates accessibility of methods for searching and screening, the coding process and its collation, yielding a succint preanalysis plan. I return to this further below. Please note, if you are merely undertaking a literature review to generate your evidence synthesis article, while this coincides with one of the broad 3 types published by PRSB, it does not necessarily equate to a formal meta-analysis, as indicated within your manuscript.
Much of the content of the constructive referee reports is self-evident, and I hope should you decide to resubmit your manuscript, will provide a useful guide of how to proceed. I would like to additionally draw your attention specifically to our requirements for publication of Evidence Synthesis articles. Notwithstanding, in your response to referees, I would be grateful if you would include a brief account relating to Editorial comments, on how the manuscript has been modified in relation to my brief suggestions. In particular, as you will have seen from the guidelines available for our Evidence Synthesis articles (https://royalsocietypublishing.org/rspb/evidence-synthesis), it is vital that the reader is able to assess the validity, robustness and objectivity of the evidence base presented. Importantly also, when putting the final touches to the article, please ensure wherever possible, that where relevant, you have addressed some of the questions below, that characterises the Evidence Synthesis article type, though I fully recognise, that many questions will only partially apply to your manuscript : 1. Is the key policy-related question(s) articulated clearly? 2. Is there a clear justification in support of policy relevance? 3. Is the likely target audience identified clearly? 4. Does the search for literature utilise a comprehensive range of sources? 5. Does the synthesis article apply clearly documented inclusion criteria to all potentially relevant studies found during the search? 6. Is a clear methodology described to avoid bias? 7. Is your study objectively weighted according to methodological quality of cited literature? 8. Are knowledge gaps and priorities clearly identified? 9. Are outcomes/recommendations tangible in terms of likely impact? 10. Are all necessary supporting information available and accessible??
Including a brief indication of how you have addressed the specific criteria above in your response letter would be most helpful. I appreciate that the volume of revision is extensive, and may go beyond what you had originally anticipated. Notwithstanding, I would hope you will find the constructive and detailed suggestions helpful in formulating a more robust and representative evidence synthesis article for resubmission. As indicated below, as in all peer review processes, the invitation to resubmit, is of course no guarantee of eventual publication, but I will do my best to exercise consistency in the remaining peer review process, by approaching the original referees, at a minimum, though of course I am not in a position to confirm their availability.

END OF EXERT FROM PREVIOUS DECISION LETTER
I appreciate that consideration of your manuscript is taking some considerable time, and of course there is no guarantee of eventual publication. I appreciate that you cannot include data that are non-existent, but equally, I remain to be sufficiently convinced, that the design and choice of data included in your analyses, have the appropriate level of transparency and robustness. It is this latter aspect that requires your attention once more. Thank you in advance for your consideration. My plan would be to return the manuscript, based on the nature of your response to one of the original reviewers, and I will select most likely a second new reviewer, so as to provide an additional final opinion.
Reviewer(s)' Comments to Author: Referee: 1 Comments to the Author(s) Sorry -you've got me again. I am still not convinced that a comparison between urban areas and a merging of rural and wildland areas is a valid comparison given rural areas may be damaging the validity of the 'control' aspects of the wildland areas. As you don't provide sample sizes for each of these treatments still, I can only assume wildland sites are scant and this is predominantly a comparison between urban areas and rural areas -which doesn't really inform us about the changes urbanisation has caused on predation patterns. Your finding of no differences between urban and rural/wildlands isn't surprising given rural lands are probably filled with anthropogenically-derived food subsidies for predators. Hence, I urge you go add in sampe sizes for both rural and wildland sites, and ideally compare each individually with urbanisation. Some minor comments: -L104-106: I think you should explain what you are comparing urban environments to.
-L231-232: How many of these 32 studies were from wildland and rural? -L311-312: I'd add 'with rural and wildland sites' to the end of this sentence -the lack of clarity regarding the comparator is challenging in reading this paper I feel.
I hope this is helpful.

Sincerely Matt
Referee: 2 Comments to the Author(s) Dear Authors, The manuscript was substantially improved, the Authors provided substantial explanation and addressed to comments in the previous review. I am satisfied with the corrections as well the answers to the reviewers. The manuscript could be accepted for publication.
Referee: 3 Comments to the Author(s) The authors have done an excellent job of responding to reviewers' concerns and suggestions. The changes to Figure 4, in particular, clearly address the concerns raised by other reviewers about the lumping of "rural" and "wildland" categories together for comparison with "urban." As I had mentioned in my comments to the editor on the original submission, these concerns are important, but the solution proposed by reviewers would have required arbitrary decisions on the part of the authors. Instead, the approach the authors have taken in this revision (comparing the delta HFI to effect sizes) is much more clear and rigorous. There is also a really nice paragraph in the discussion (lines 324-343) that describes the complexity of doing comparative studies, given the complexity and heterogeneity inherent in cities' surrounding landscapes.
I have only the most minor of editorial comments on this version: Line 304 -change "out" to "our" Line 326 -change predator's to predators' (if I'm reading this correctly) Line 364 -run-on sentence; needs a break between "extinctions" and "it", I think Line 374 -change revealed to reveal (or change tense of the first part of the sentence) Author's Response to Decision Letter for (RSPB-2021-1205.R0)

Recommendation
Accept with minor revision (please list in comments)

General interest: Is the paper of sufficient general interest? Good
Quality of the paper: Is the overall quality of the paper suitable? Good

Do you have any concerns about statistical analyses in this paper? If so, please specify them explicitly in your report. No
It is a condition of publication that authors make their supporting data, code and materials available -either as supplementary material or hosted in an external repository. Please rate, if applicable, the supporting data on the following criteria.

Do you have any ethical concerns with this paper? No
Comments to the Author Dear Authors, The manuscript is interesting and brings valuable information about trophic ecology in the anthropogenic context. The Authors provided substantial explanations why they segregated rural and wildland areas and the fact that for some taxa the number of relevant results was not satisfactory. However, I have slight suggestions and minor corrections which could be provided by the Authors. The most important is the title. "Diet" sounds too general. In my opinion the Authors should mention predation or predators, as it is the only trophic interaction studied in the work and also as the introduction begins with "predation." This implies the importance of it and the further flow of the manuscript. L193 -198 -I would move the majority of this description to introduction (L 106-107) P 8 vs -use italics P 10 L 180 -186 -the explanation for MLE -I would included it only once in the "statistical analysis" only L 412 -415 -I suggest to move recommendation to the very last conclusion I would like to see the captions for the supplementary material, there should table 1 and figures S1, S2, there is one file with graphs and one excel csv table

Review form: Reviewer 3
Recommendation Accept with minor revision (please list in comments)

General interest: Is the paper of sufficient general interest? Excellent
Quality of the paper: Is the overall quality of the paper suitable? Excellent

Is the length of the paper justified? Yes
Should the paper be seen by a specialist statistical reviewer? No Do you have any concerns about statistical analyses in this paper? If so, please specify them explicitly in your report. No It is a condition of publication that authors make their supporting data, code and materials available -either as supplementary material or hosted in an external repository. Please rate, if applicable, the supporting data on the following criteria.

Comments to the Author
The revisions have taken an already important and impactful paper and have made it even clearer. I appreciate the thoughtful responses of the authors to the most recent set of reviews and editorial comments. I think their additions to the methods and analyses fully address the reviewers' and editor's concerns. I have only a couple of minor points of clarification that I would like to see in the new text. I emphasize again my disagreement with some of the suggestions made by reviewer #1 in particular, though I (like the authors) have become convinced that including some additional detail about the non-urban reference sites is helpful for readers.
In my previous reviews and correspondence with the editor about this study, I was critical of reviewer #1's suggestion of separating the non-urban site types into the categories of 'rural' and 'wildland.' These categories are even more poorly defined in the literature than is 'urban' (see references below). I think the authors' new analyses bear this out: i.e. the complete overlap of studies with rural and wildland sites as their non-urban reference in the effect size plots included in this new version of the manuscript. However, I think the authors have done a nice job of threading that needle -including some additional detail about how the non-urban site conditions varied among studies, while also contextualizing the inherent complexity in the discussion. Providing the summary number of studies with rural (agricultural) vs. wildland (protected areas/wilderness areas) is helpful for readers. I still maintain that the HFI, as a standardized quantitative measure of human influence, is the best way to characterize the non-urban sites and the variation among studies.
Given these new inclusions, I think it would be helpful to make two additional clarifications (just a sentence needed for each): 1.
Clarify what information was used for this additional categorization of sites as rural vs. wildland. Verbal description of the sites in the original study? examination of their maps? 2.
Include a summary of the HFI scores for the new rural vs. wildland categories.

Review form: Reviewer 4
Recommendation Major revision is needed (please make suggestions in comments)

Scientific importance: Is the manuscript an original and important contribution to its field? Acceptable
General interest: Is the paper of sufficient general interest? Acceptable Quality of the paper: Is the overall quality of the paper suitable? Acceptable Is the length of the paper justified? Yes

Do you have any concerns about statistical analyses in this paper? If so, please specify them explicitly in your report. No
It is a condition of publication that authors make their supporting data, code and materials available -either as supplementary material or hosted in an external repository. Please rate, if applicable, the supporting data on the following criteria.

Do you have any ethical concerns with this paper? No
Comments to the Author General comments I did not review this previously, but it appears that it is a resubmission. I think there is still room for further improvement. In the present study, a global meta-analysis of the effects of urbanisation on diet patterns of vertebrate predators was conducted. The authors found difficulties in assigning 'urban' and attempted to make comparisons with 'rural' or 'natural areas. Some recent literature shows that some urban landscapes are mosaics with patches of green spaces (natural and managed) that often allow the persistence of certain species, including predators, making comparisons more difficult. It may be better for some species to compare what was considered their natural diet with what they are feeding on in the urban landscape mosaic.
The authors' initial search yielded 358 studies covering a range of vertebrate taxa for the period (1986-2020). Concerning was how few studies were found in the southern hemisphere and that none were found for Africa. There definitely have been some urban diet studies of predators in African cities during this time. However, it is not clear if they only used studies where there was a comparison across a gradient. Also, many of the northern hemisphere studies focus on relatively few predators but have many studies on those species, and that is not reflected in your results.
Also, one of the issues in urban environments is the increase in certain prey species (Discussion L340-343). Some species may appear more specialised in their diet (Results L277), but it is likely the availability of certain prey types (Results L284), so these cannot be assessed independently.
There is no mention of increased anthropogenic pollution in the diet of some of the urban predators, but this has been reported in some studies.
I found the manuscript generally well written. Perhaps replace 'taxonomic group' with 'taxa' throughout. I suggest replacing 'due to' with 'because of' throughout. Also, replace 'compared to' with 'compared with' or 'than'. Also, where 'mammal' or 'reptile' are adjectives rather change to 'mammalian' and 'reptilian'. Generally, Figure and

Introduction:
A generally good synthesis of the relevant literature. However, I think you need to mention that some of the urban landscapes are mosaics with patches of green spaces (natural and managed) that often allow the persistence of certain predatory species. L79 I think you should is the increase in certain prey species (Discussion L340-343) here. L105-129 Although Journals historically used the present tense for this, there is a trend to use past tense as the work is done and it reads better. L123 remove parentheses from HFI.

Methods:
Good explanation of methods used. My only concern was the isotope data. Did you use studies that presented these data only, or did you convert some of the other diet studies based on the typical isotopic signature? If the former, you need to present how many studies there were in your results. Decision letter (RSPB-2021-2487.R0)

05-Jan-2022
Dear Ms Gámez: Your manuscript has now been peer reviewed and the reviews have been assessed by an Associate Editor. The reviewers' comments (not including confidential comments to the Editor) and the comments from the Associate Editor are included at the end of this email for your reference. As you will see, the reviewers and the Editors have raised some concerns with your manuscript and we would like to invite you to revise your manuscript to address them.
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Best wishes, Dr The Proceedings B Team mailto: proceedingsb@royalsociety.org Associate Editor Board Member Comments to Author: Thank you for your detailed and constructive response to the previous round of editorial and referee comments. I certainly appreciate, as did the reviewers, the effort expended in the resubmitted version, as well as the helpful response to the variety of substantive issues raised. I am pleased to say that collectively, there is a consensus that the manuscript has improved significantly, and that the additional details, especially in the methodology, has generated a more rigourous and robust evidence base. I appreciate that revisions cannot extend remorselessly, though I do feel there is additional benefit to a further consideration of new comments below.
First, I acknowledge the point by point responses to my editorial comments, especially those relating to methodology and the various criteria that characterise the evidence synthesis framework. Overall, I am satisfied that you have achieved the appropriate level of information and approach. I would like to invite you to consider some remaining points, including your usage of the word "diet" in the title, and whether a more explicit link to predation or predators might be more appropriate. Your reconsideration of the use of landtype categories, esp. rural and wildland is now more substantiated, though there are suggestions, with only brief additional detail, concerning the additional categorisation of sites, and the inclusion of a summary of the HFI scores for the new rural vs. wildlife categories. In this context, you will see comments referring to the possible inclusion of mosaics with patches of green spaces, and the impact of likely lack of independence between some factors, such as diet specialisation and the availability of certain prey items. Some very constructive additional suggestions are made by the referees that I think you will find both informative and appropriate in what I envisage as a final round of revision.
It is unlikely that I will need to send your manuscript out for further review, but I would appreciate a brief uploaded response letter, with a summary of key issues and the associated changes made. Thank you again for the care and effort in generating the resubmission, your valuable aid in navigating the primary changes, and importantly, your efforts in complying with our evidence synthesis format. While you will see various suggestions made, I would hope that they would require relatively little additional time, and I hope you will be in a position to revise your manuscript in the near future. I look forward to seeing a revised version in due course.
Reviewer(s)' Comments to Author: Referee: 4 Comments to the Author(s). General comments I did not review this previously, but it appears that it is a resubmission. I think there is still room for further improvement. In the present study, a global meta-analysis of the effects of urbanisation on diet patterns of vertebrate predators was conducted. The authors found difficulties in assigning 'urban' and attempted to make comparisons with 'rural' or 'natural areas. Some recent literature shows that some urban landscapes are mosaics with patches of green spaces (natural and managed) that often allow the persistence of certain species, including predators, making comparisons more difficult. It may be better for some species to compare what was considered their natural diet with what they are feeding on in the urban landscape mosaic.
The authors' initial search yielded 358 studies covering a range of vertebrate taxa for the period . Concerning was how few studies were found in the southern hemisphere and that none were found for Africa. There definitely have been some urban diet studies of predators in African cities during this time. However, it is not clear if they only used studies where there was a comparison across a gradient. Also, many of the northern hemisphere studies focus on relatively few predators but have many studies on those species, and that is not reflected in your results.
Also, one of the issues in urban environments is the increase in certain prey species (Discussion L340-343). Some species may appear more specialised in their diet (Results L277), but it is likely the availability of certain prey types (Results L284), so these cannot be assessed independently.
There is no mention of increased anthropogenic pollution in the diet of some of the urban predators, but this has been reported in some studies.
I found the manuscript generally well written. Perhaps replace 'taxonomic group' with 'taxa' throughout. I suggest replacing 'due to' with 'because of' throughout. Also, replace 'compared to ' with 'compared with' or 'than'. Also, where 'mammal' or 'reptile' are adjectives rather change to 'mammalian' and 'reptilian'. Generally, Figure and

Introduction:
A generally good synthesis of the relevant literature. However, I think you need to mention that some of the urban landscapes are mosaics with patches of green spaces (natural and managed) that often allow the persistence of certain predatory species. L79 I think you should is the increase in certain prey species (Discussion L340-343) here. L105-129 Although Journals historically used the present tense for this, there is a trend to use past tense as the work is done and it reads better. L123 remove parentheses from HFI.
Methods: Good explanation of methods used. My only concern was the isotope data. Did you use studies that presented these data only, or did you convert some of the other diet studies based on the typical isotopic signature? If the former, you need to present how many studies there were in your results. In my previous reviews and correspondence with the editor about this study, I was critical of reviewer #1's suggestion of separating the non-urban site types into the categories of 'rural' and 'wildland.' These categories are even more poorly defined in the literature than is 'urban' (see references below). I think the authors' new analyses bear this out: i.e. the complete overlap of studies with rural and wildland sites as their non-urban reference in the effect size plots included in this new version of the manuscript. However, I think the authors have done a nice job of threading that needle -including some additional detail about how the non-urban site conditions varied among studies, while also contextualizing the inherent complexity in the discussion. Providing the summary number of studies with rural (agricultural) vs. wildland (protected areas/wilderness areas) is helpful for readers. I still maintain that the HFI, as a standardized quantitative measure of human influence, is the best way to characterize the non-urban sites and the variation among studies.
Given these new inclusions, I think it would be helpful to make two additional clarifications (just a sentence needed for each): 1. Clarify what information was used for this additional categorization of sites as rural vs. wildland. Verbal description of the sites in the original study? examination of their maps? 2. Include a summary of the HFI scores for the new rural vs. wildland categories.

Is it clear? Yes
Is it adequate? Yes

Do you have any ethical concerns with this paper? No
Comments to the Author Thanks for addressing my comments.

28-Jan-2022
Dear Ms Gámez I am pleased to inform you that your manuscript entitled "Downtown Diet: a global metaanalysis of increased urbanization on the diets of vertebrate predators" has been accepted for publication in Proceedings B.
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