Fungicides, herbicides and bees: A systematic review of existing research and methods

Merissa G. Cullen; Linzi J. Thompson; James. C. Carolan; Jane C. Stout; Dara A. Stanley

doi:10.1371/journal.pone.0225743

Peer Review History

Original SubmissionJuly 28, 2019
13 Sep 2019 Decision Letter - James C. Nieh, Editor PONE-D-19-21233 Fungicides, Herbicides and bees: A systematic review of existing research and methods PLOS ONE Dear Dr Stanley, Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process. Although Reviewer 2 recommended reject, I think that the comments could be addressed in a major revision, particularly, the concerns of better summarizing the results of these studies. We would appreciate receiving your revised manuscript by Oct 28 2019 11:59PM. When you are ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file. 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Please do not edit.] Reviewers' comments: Reviewer's Responses to Questions Comments to the Author 1. 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 ******** 2. Has the statistical analysis been performed appropriately and rigorously? Reviewer #1: N/A Reviewer #2: Yes ****** 3. 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 ****** 4. 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 ******** 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: Cullen et al. PLOSONE In the paper entitled “Fungicides, Herbicides and bees: A systematic review of existing research and methods” the authors adopted a systematic approach to review existing research on the potential impacts of fungicides and herbicides on bees. The study is very interesting and topical since many recent studies highlighted the potential direct or indirect impact of fungicides and herbicides on bee health (e.g. Simon-Delso et al. 2014 PlosOne; Motta et al. 2018 PNAS). I found the methods adequate and the results clearly presented. Minor comments: L153-157: Maybe you missed the geographical distribution of one study. You have 90 studies but 43+30+8+6+1+1=89. Please, double-check the information reported in this paragraph and in the figure 1; L213-217: Here, you provide the information on the life stage that the studies focused on but it would be interesting to also know in which stage the bees were exposed to pesticides; L274-278: Differences in life history traits between honey bees and solitary bees may also determine differences in routes and levels of pesticide exposure. These differences were recently highlighted in a Workshop on ‘Pesticide Exposure Assessment Paradigm for non-Apisbees’ held in 10–12 January 2017, at the United States Environmental Protection Agency (USEPA) in Arlington, Virginia (USA) and published in a special collection (https://academic.oup.com/ee/pages/pesticide_exposure_in_non-honey_bees). L285: Please, add the percentage of studies that investigated sub-lethal effects; Table 3 and 4: Add a column with the pesticide group for each compound. Reviewer #2: In “Fungicides, Herbicides and bees: A systematic review of existing research and methods”, the authors summarize what types of studies have investigated the impact of fungicides and herbicides on bees. Given their findings, the authors argue that further work must be done on non-honey bees as well as sub-lethal effects of fungicides and herbicides (which are generally less studied than neonic pesticides). Major comment: Although this review succeeds at illuminating that more work should be done on the effects of fungicides and herbicides on bees, it would be greatly improved by including a summary of the results of the studies. Do fungicides and herbicides affect bees? A review of this nature would add greatly to the knowledge about the effect of fungicides and herbicides on bees by synthesizing the findings of the reviewed studies, rather than only summarizing what methods prior research has employed. In its current state, this review is incomplete. The addition of a synthesis and summary of how fungicides and herbicides affect bees will greatly improve the manuscript and fill many of the gaps of knowledge the authors argue need filling. Minor comments: Line 25: have been -Line 46 and throughout the entire document: It is unclear when you say “bees” whether you are referring to honey bees specifically or all species of bees. In most cases it seems to be in reference to honey bees, but at other times it is more general. -Some of the questions outlined in the intro are unclear or hard to understand. Clearer wording would make this more helpful: -Line 68: I do not understand question (i). Does ‘when’ mean year, season, stage of bee lifecycle? Does ‘where’ mean part of the world, type of crop, etc.? -Line 71: What is the meaning of “formulation” in this context? -Line 97: Why did you not include observational data? I would think that observations of declines in bee communities would be important to an understanding of how fungicides and herbicides affect bees. A justification for this omittance should be included. -Line 117: Forgot to include definition of ‘model’ studies. -Line 144: Please elucidate what a ‘consumption effect’ is. -Line 215: Were studies that looked at egg, pupa, and larvae exclusive to honey bee studies, or were these common for other species as well? ******* 6. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files. If you choose “no”, your identity will remain anonymous but your review may still be made public. Do you want your identity to be public for this peer review?** For information about this choice, including consent withdrawal, please see our Privacy Policy. Reviewer #1: Yes: Fabio Sgolastra Reviewer #2: No [NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files to be viewed.] While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email us at figures@plos.org. Please note that Supporting Information files do not need this step. https://doi.org/10.1371/journal.pone.0225743.r001
Revision 1
30 Oct 2019 Author Response esponses to Review Comments to the Author Reviewer #1: Cullen et al. PLOSONE In the paper entitled “Fungicides, Herbicides and bees: A systematic review of existing research and methods” the authors adopted a systematic approach to review existing research on the potential impacts of fungicides and herbicides on bees. The study is very interesting and topical since many recent studies highlighted the potential direct or indirect impact of fungicides and herbicides on bee health (e.g. Simon-Delso et al. 2014 PlosOne; Motta et al. 2018 PNAS). I found the methods adequate and the results clearly presented. Minor comments: L153-157: Maybe you missed the geographical distribution of one study. You have 90 studies but 43+30+8+6+1+1=89. Please, double-check the information reported in this paragraph and in the figure 1; This has now been checked and rectified. L213-217: Here, you provide the information on the life stage that the studies focused on but it would be interesting to also know in which stage the bees were exposed to pesticides; Here we have already included data no both the life-stage that the bees were exposed to pesticides and the life-stage at which effects were measured. We have clarified this now in the methods section as follows: “If the life stages at which bees were exposed to pesticides different to the life stage at which effects were measured, then both were included in final analyses”. L274-278: Differences in life history traits between honey bees and solitary bees may also determine differences in routes and levels of pesticide exposure. These differences were recently highlighted in a Workshop on ‘Pesticide Exposure Assessment Paradigm for non-Apisbees’ held in 10–12 January 2017, at the United States Environmental Protection Agency (USEPA) in Arlington, Virginia (USA) and published in a special collection (https://academic.oup.com/ee/pages/pesticide_exposure_in_nonhoney_ bees). We thank the reviewer for pointing this out, and have now cited two of these papers at this point within the manuscript (L292). L285: Please, add the percentage of studies that investigated sub-lethal effects; This has been added as suggested (L296 & L299) Table 3 and 4: Add a column with the pesticide group for each compound. These columns have now been added as suggested Reviewer #2: In “Fungicides, Herbicides and bees: A systematic review of existing research and methods”, the authors summarize what types of studies have investigated the impact of fungicides and herbicides on bees. Given their findings, the authors argue that further work must be done on non-honey bees as well as sub-lethal effects of fungicides and herbicides (which are generally less studied than neonic pesticides). Major comment: Although this review succeeds at illuminating that more work should be done on the effects of fungicides and herbicides on bees, it would be greatly improved by including a summary of the results of the studies. Do fungicides and herbicides affect bees? A review of this nature would add greatly to the knowledge about the effect of fungicides and herbicides on bees by synthesizing the findings of the reviewed studies, rather than only summarizing what methods prior research has employed. In its current state, this review is incomplete. The addition of a synthesis and summary of how fungicides and herbicides affect bees will greatly improve the manuscript and fill many of the gaps of knowledge the authors argue need filling. While we agree that it would be very useful to have a review on the effects of fungicides and herbicides on bees, we think that that is beyond the scope of the current paper. The best way to do this is to perform a meta-analysis, using effect sizes from a number of studies to make a broad conclusions as to whether these compounds have effects or not. However, our review shows that there is not a lot of studies investigating effects of herbicides and fungicides on bees overall, and where there are they vary hugely in terms of compounds studied, concentrations used, and bee species studied. To perform a proper meta-analysis you need a cohort of studies investigating a similar question so that they can be compared and summarised in a meaningful way. This simply does not exist in this body of literature yet, and we have clarified this further in the discussion (L387- 399). There are many other existing studies that, like ours, summarise research approaches and methods rather than effects (e.g. Lundin et al. 2015 Plos One), and this is often the first step towards a more detailed meta-analysis later on when the existing body of literature has further developed. Although a full evaluation of effects is not possible, we agree with the reviewer that a higher level summary of effects would be useful and so we have added details of the main findings of each paper in S3 Table B in the supplementary materials. Minor comments: Line 25: *have been This has been corrected -Line 46 and throughout the entire document: It is unclear when you say “bees” whether you are referring to honey bees specifically or all species of bees. In most cases it seems to be in reference to honey bees, but at other times it is more general. In general, wherever we use this term we are referring to all bees. We have clarified this at this point as suggested here (L47), and also in line 226-230. -Some of the questions outlined in the intro are unclear or hard to understand. Clearer wording would make this more helpful: We have tried to clarify this where possible and have also referred to Table 1 here that provides a more detailed description of the variables used in each question. -Line 68: I do not understand question (i). Does ‘when’ mean year, season, stage of bee lifecycle? Does ‘where’ mean part of the world, type of crop, etc.? We have clarified this and it now reads “In what year and in what geographical location has existing research has taken place?” -Line 71: What is the meaning of “formulation” in this context? We have clarified this as follows: “commercially produced pesticide formulation” -Line 97: Why did you not include observational data? I would think that observations of declines in bee communities would be important to an understanding of how fungicides and herbicides affect bees. A justification for this omittance should be included. Observational data is usually based on correlations. Therefore, it is never clear whether any patterns observed are directly due to pesticide use or perhaps some other intermediary factor. We have now clarified this further here (L103-104). -Line 117: Forgot to include definition of ‘model’ studies. This has now been added -Line 144: Please elucidate what a ‘consumption effect’ is. This has now been clarified “consumption (e.g. ability to consume nectar and/or pollen)” -Line 215: Were studies that looked at egg, pupa, and larvae exclusive to honey bee studies, or were these common for other species as well? We have now added in the following text in response to this question: “Egg studies were only carried out on Megachile rotundata, whereas larval and pupal studies involved multiple bee species https://doi.org/10.1371/journal.pone.0225743.r002
12 Nov 2019 Decision Letter - James C. Nieh, Editor Fungicides, Herbicides and bees: A systematic review of existing research and methods PONE-D-19-21233R1 Dear Dr. Stanley, We are pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it complies with all outstanding technical requirements. Within one week, you will receive an e-mail containing information on the amendments required prior to publication. When all required modifications have been addressed, you will receive a formal acceptance letter and your manuscript will proceed to our production department and be scheduled for publication. Shortly after the formal acceptance letter is sent, an invoice for payment will follow. To ensure an efficient production and billing process, please log into Editorial Manager at https://www.editorialmanager.com/pone/, click the "Update My Information" link at the top of the page, and update your user information. If you have any billing related questions, please contact our Author Billing department directly at authorbilling@plos.org. If your institution or institutions have a press office, please notify them about your upcoming paper to enable them to help maximize its impact. If they will be preparing press materials for this manuscript, you must inform our press team as soon as possible and no later than 48 hours after receiving the formal acceptance. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org. With kind regards, James C. Nieh, Ph.D. Academic Editor 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 #2: All comments have been addressed ******** 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 #2: Yes ****** 3. Has the statistical analysis been performed appropriately and rigorously? Reviewer #2: Yes ****** 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 #2: Yes ****** 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 #2: Yes ****** 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 #2: (No Response) ****** 7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files. If you choose “no”, your identity will remain anonymous but your review may still be made public. Do you want your identity to be public for this peer review?** For information about this choice, including consent withdrawal, please see our Privacy Policy. Reviewer #2: No https://doi.org/10.1371/journal.pone.0225743.r003
Formally Accepted
3 Dec 2019 Acceptance Letter - James C. Nieh, Editor PONE-D-19-21233R1 Fungicides, Herbicides and bees: A systematic review of existing research and methods Dear Dr. Stanley: I am pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department. If your institution or institutions have a press office, please notify them about your upcoming paper at this point, to enable them to help maximize its impact. If they will be preparing press materials for this manuscript, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org. For any other questions or concerns, please email plosone@plos.org. Thank you for submitting your work to PLOS ONE. With kind regards, PLOS ONE Editorial Office Staff on behalf of Dr. James C. Nieh Academic Editor PLOS ONE https://doi.org/10.1371/journal.pone.0225743.r004

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