PONE-D-24-49004Where the wild bees are: birds improve indicators of bee richnessPLOS ONE

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Reviewers' comments:

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Comments to the Author

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Reviewer #1: Yes

Reviewer #2: Yes

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2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: I Don't Know

Reviewer #2: Yes

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3. Have the authors made all data underlying the findings in their manuscript fully available?

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Reviewer #1: Yes

Reviewer #2: Yes

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Reviewer #1: Yes

Reviewer #2: Yes

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5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: Revision: Where the wild bees are: birds improve indicators of bee richness

This manuscript investigates the performance of environmental and bird-based indicators in predicting wild bee richness in the U.S. The authors provide robust evidence that birds enhance the predictive power of land cover data as indicators of wild bee richness. The manuscript explores a novel and interesting approach (I was not familiar with) that is highly relevant to a broad audience, particularly conservationists focused on wild bees. Given that bird occurrence and diversity data are often far more extensive than comparable data for wild bees, this study addresses a significant knowledge gap.

The text is well-structured and well-written, with a particularly engaging introduction. The discussion is nuanced, effectively highlighting the strengths of the study while addressing its limitations. I support this manuscript for publication, subject to addressing the minor comments detailed below.

Abstract

• Line 23: “Widespread declines in wild bee populations necessitates”—either remove the “s” from “declines” or from “necessitates” to correct the subject-verb agreement.

Introduction

• Line 47: A closing parenthesis appears to be missing.

• Line 55: There is a double space between “them.” and “Consequently.”

• Lines 80–82: The distinction between ‘environmental health’ and ‘environmental quality’ is unclear. Are there rigorous definitions that differentiate these terms? Additionally, the statement that invertebrates are better proxies for one and birds for the other requires more explanation or supporting references.

• Lines 86–93: These lines, discussing the use of single species or assemblages, directly relate to concepts introduced in lines 74–76. Consider merging lines 74–76 with lines 86–93 for a more cohesive discussion, and then proceed with lines 76–86, which focus on specific taxa and their relevance.

• Lines 113–114: There seems to be another missing parenthesis in this section.

Methods

• Lines 149–151: I am not sure how bee richness was calculated. Specifically, how did you integrate data from net sampling when averaging the number of species per trap per survey? Further clarification on this methodology would be helpful.

• Lines 164–165: This might be a naïve observation, but in this semi-structured dataset, surveys appear to follow different protocols. Couldn’t this lead to significant variations in the number of species per survey, not due to actual differences in species richness, but as a result of methodological discrepancies? For instance, depending on the sampling method (e.g., nets, traps, or nets + traps) or the sampling duration, the number of species recorded at the same site on the same day can vary substantially; it can easily double or triple. How do you think this variability might influence the trends observed in your study? Additionally, why did you use the mean instead of the median to summarise species richness? Wouldn’t the median reduce the influence of outliers? Alternatively, why not consider the total number of species observed across all surveys within a grid cell?

• Line 170: Why did you not include pre-nuptial migration periods, such as April, in your bird-based index? April is a critical period for many early-season bee species, and excluding it might overlook their habitat requirements. Including data from pre-nuptial migration sites and their associated bird diversity could potentially improve the index's applicability to early-season bees. While, of course, re-extracting bird data is beyond the scope of this study, do you think this aspect is worth exploring in future research?

Discussion

• Line 333: It seems that a track change was not removed, specifically in the space between “bees” and (101).

Figures

• Figure 2: In the figure legend, could you clarify what “scaled uncertainty” represents? Is it expressed as a percentage or as a number of species?

• Figure 2: It might be valuable to include a map showing actual bee richness based on existing data. This would allow for a direct comparison between observed richness and the predicted values, providing additional context and insight into the model's accuracy.

Thanks for this great paper, as a bee researcher, and a bird lover, I particularly enjoyed it !

Maxence Gérard

Reviewer #2: The article presents an interesting case of searching for an improved performance of land use predictors, when combined with citizen science bird databases, to indicate species richness of wild bees. It's aim is using the former as indicators of the less know biodiversity of the latter.

In my opinion, the research has a good design and a solid methodological approach that makes its publication highly recommended.

There are only a few suggestions on how to express certain issues included in the introduction, discussion and conclusions, which I propose to the authors for their consideration. These questions relate more to the wording of these three sections and possible improvements in the formulation and interpretation of the hypotheses and results, than to methodological issues that, as I have indicated, are adequately described and justified in their choice and application.

1) The statement (lines 99 – 101) “however, to our knowledge, González et al. (17) and Fleishman et al. (27) were first to document that a combination of environmental variables and indicator species best explained restoration success and variation in species richness, respectively”, is a bit confusing. Since it is unlikely that these are the only that have adopted this approach (as one might think), it would be convenient to cite at this point some additional references published after them that can be considered background to the present research.

2) If anything, in relation to the methodology, I would appreciate an explanation in some detail of the methodological basis of the eBird product cited (reference 92, Fink et al., 2021: Lines 250-252 “we needed estimates of relative bird abundance in all grid cells, not only those with eBird checklists, therefore we used the estimated relative abundance per species per grid cell from eBird Status Data Products (92)”. Although this product is explained in the link associated to the reference, it seems appropriate that the authors (and not the reader) be the ones to extract -and include in the text- this necessary methodological note.

3) Lines 350-350: The sentence "Fourth, the combined bird and land cover variables selected as predictors represent a wide range of habitats, which suggest that a higher bee richness may be associated with heterogeneous landscapes (110–112) that include multiple types of nesting substrates to accommodate ground and cavity nesters and a diversity of flower resources, from crops, shrubs, and trees", is also a bit confusing since the argument combines nesting substrates (¿for birds?) and trophic resources (for bees? for both?). The relationship of birds with heterogeneous landscapes and structurally diverse habitats, and their consequent indicator value for habitat diversity for pollinators, should probably be differentiated. Likewise, it should be accompanied by some references that support the first relationship, since all those cited (110-112) refer exclusively to the habitat relationships of pollinators.

On the contrary, in the sentence between lines 392-394, which refers entirely to pollinators, "The structured dataset included protocol and effort information, enabling us to generate more precise bee richness estimates across space (121,122)", the second reference cited is on birds. It is not clear to me what justifies its use.

4) The article goes into little detail about the cautions to be taken when choosing birds as surrogate for invertebrates (wild pollinators in this case), especially taking into account the extensive literature on the lack of correspondence between protected areas designated with criteria based on each of these taxocenoses. For example, the following works or others with a similar approach can be cited:

- Guareschi, S., Abellán, P., Laini, A., Green, A. J., Sánchez-Zapata, J. A., Velasco, J., & Millán, A. (2015). Cross-taxon congruence in wetlands: assessing the value of waterbirds as surrogates of macroinvertebrate biodiversity in Mediterranean Ramsar sites. Ecological Indicators, 49, 204-215.

- Oberprieler, S. K., Andersen, A. N., Gillespie, G. R., & Einoder, L. D. (2019). Vertebrates are poor umbrellas for invertebrates: cross‐taxon congruence in an Australian tropical savanna. Ecosphere, 10(6), e02755.

- Rooney, R. C., & Bayley, S. E. (2012). Community congruence of plants, invertebrates and birds in natural and constructed shallow open-water wetlands: do we need to monitor multiple assemblages?. Ecological Indicators, 20, 42-50. (This last article raises as a final remark that cross-congruence between taxocenoses may be reduced in degraded ecosystems with respect to those that maintain a good level of conservation, which may also be a relevant aspect to consider here)

5) The conclusions section is this respect somewhat vague; it should specify a little more what type of conservation measures are recommended, since the selection of areas to be protected does not guarantee a great concordance between those aimed at birds and those that can protect other taxa.

In particular, studies have shown a mismatch between existing protected areas (essentially designated on the basis of plant or vertebrate taxa) and areas of modelled high diversity of wild bees (e.g. Casanelles‐Abella, J., Fontana, S., Meier, E., Moretti, M., & Fournier, B. (2023). Spatial mismatch between wild bee diversity hotspots and protected areas. Conservation Biology, 37(4), e14082.)

6) Moreover, the claim that birds can help identify areas rich in wild bee species through their indication of habitat diversity could be criticized, at least partly, on the basis of other research not reported by the authors, e.g. Geue JC, Rotter PJ, Gross C, Benkő Z, Kovács I, Fântână C, et al. (2022) Limited reciprocal surrogacy of bird and habitat diversity and inconsistencies in their representation in Romanian protected areas. PLoS ONE 17(2): e0251950. https://doi.org/10.1371/journal.pone.0251950

In addition, i found thes minor observations/corrections referring to specific lines of the manuscript:

Lines 330-333: “For example, numbers of flowering plants that attract bees are often greater in early-successional than mature forests(97). Likewise, forests in which understories were replaced by manicured lawn (e.g., wooded parks) provide less floral resources to bees_(101).

- There is a space missing between "mature forest" and "(97)"

- The space between "...floral resources to bees" and "(101)" does not need to be underlined

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Reviewer #1: Yes:  Maxence Gérard

Reviewer #2: No

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Where the wild bees are: birds improve indicators of bee richness

PONE-D-24-49004R1

Dear Dr. Rousseau,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

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PLOS ONE

Additional Editor Comments (optional):

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: All comments have been addressed

Reviewer #2: All comments have been addressed

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2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

Reviewer #2: Yes

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3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: Yes

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4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

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5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

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6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: Dear Authors,

Thank you for your revision. I have no additional comments and fully support the acceptance of this paper.

Best regards,

Maxence Gérard

Reviewer #2: (No Response)

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Reviewer #1: Yes:  Maxence Gérard

Reviewer #2: No

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