By Methods in Ecology and Evolution Executive Editor Aaron M. Ellison
A recent Practical Tools article published in Methods in Ecology & Evolution described a foot snare used to capture jaguars and cougars in Brazil (Ribeiro de Araujo et al. 2021a). Within hours of the posting of the proofed version of the article on the Early View section of the journal’s website, comments on Twitter called into question the authors’ ethics and standards for animal welfare, the associated peer-review process, editorial oversight at the journal, and its standards and requirements with respect to animal welfare. As the Senior Editor responsible for managing Ribeiro de Araujo et al.’s submission and eventually accepting the manuscript for publication, I responded as quickly as possible on Twitter to the key issues raised. I subsequently invited the submission to the journal of a commentary on the article. The commentary (Caravaggi et al. 2021) and the response to it (Ribeiro de Araujo et al. 2021b) were published this week.
In their commentary, Carvaggi et al. (2021) raise issues regarding details omitted by Ribeiro de Araujo et al. (2021a), present apparent shortcomings in the review process and journal policies, and suggest improved practices for publications involving the use of vertebrate animals in research. In their reply, Ribeiro de Araujo et al. (2021b) respond effectively to the issues regarding methodological details. Here, I review and discuss the process leading to the publication of Ribeiro de Araujo et al. (2021a). I then highlight key changes made across the BES journals in response to the points raised by Caravaggi et al. (2021) and others.
Ribeiro de Araujo et al. initially submitted their manuscript as a full-length research article. A Senior Editor of the journal evaluates every submission to determine whether it is within the scope of the journal, is likely to be of broad interest to our general readership, and is sufficiently novel and technically sound so that it has a reasonable likelihood of making it through the review process. The four Senior Editors of Methods in Ecology and Evolution have broad interests and specific areas of expertise, but none of us are specialists in every field and our initial evaluations are based on many factors, both subjective and objective.
When I evaluated Ribeiro de Araujo et al.’s initial submission, it was my opinion that the manuscript did not present a sufficiently novel or large enough methodological advance to warrant publication as a full research article. How did I arrive at this opinion? Foot snares were developed many decades ago as an alternative to earlier and more harmful methods of capturing large felids using box traps and trained hounds. Foot snares have been used widely for more than two decades and their benefits for reducing risk and potential for causing harm have been widely discussed. Ribeiro de Araujo et al. were fully aware of this literature; indeed, the initial submission of the full-length research article included descriptions and numbers of relevant permits issued by two different review boards in Brazil and detailed discussion of animal welfare issues raised by foot snares, reduced likelihood of injuries, and information on the one animal that suffered a paw injury after it was snared.
The authors had clearly been diligent with respect to ethical behavior and concern for animal welfare. But the key point of Ribeiro de Araujo et al.’s submission was to describe modest improvements to the design of foot snares used to capture African lions to enable their use in Brazil. I felt that the design improvements, the detailed diagrams, and the applicability of the system on another continent together could be presented better in the Practical Tools format without detailed discussion of all the animal welfare issues that had been discussed elsewhere in the literature. I thus “desk-rejected” their initial submission and invited a resubmission of the paper as a shorter, Practical Tools contribution.
The permit numbers unfortunately were not included in the Practical Tools submission. The BES’s editorial policy on animal ethics in place at the time requested that authors include relevant permit numbers in the Acknowledgements section, but this was not routinely checked by the Senior Editors or staff in our editorial office. Many of the details about animal welfare and injuries also were omitted from the Practical Tools submission—and with perfect hindsight, it is unfortunate that these details weren’t included in an online supplement—but this too was understandable as guidelines for this type of short article specify that authors should describe:
new field techniques, equipment or lab protocols. Articles need to clearly demonstrate how tools designed for specific systems or problems can be adapted for more general use. Online supporting information may include specific instructions, especially for building equipment.
Further, the submission process at the time for all article types (including Practical Tools) required only that authors declare (via online checkbox) that
The work conforms to the legal requirements of the country in which it was carried out, including those relating to conservation and welfare, and to the journal’s policy on these matters.
The authors affirmed this, and the submission moved forward into the review process.
From there, the review and publication process proceeded without incident (note that as part of the commitment of the journal and the BES to transparent, open science, the complete set of reviews, responses, and decisions is available online through Publons). The reviews of the paper were uniformly positive. During the initial round of review, the two anonymous reviewers and an Associate Editor all agreed that the paper would be a valuable contribution to the field. Neither the reviewers nor the Associate Editor commented on the missing permit numbers and only Reviewer 2 asked for some additional discussion of potential risks of harm. In synthesizing the reviews, the Associate Editor identified key points the authors needed to consider in their revision: “relatively minor clarifications, especially for the figures and detailed pictures of the snare method, and also language editing.” Taking all the comments and recommendations into account, I asked the authors for a minor revision of the manuscript. As the authors revised their manuscript in line with all the suggestions, with particular emphasis on those points raised by the Associate Editor, the revision was accepted for publication. It was only after the paper had been typeset and posted that the need for additional detail and discussion was raised.
The first request was for more information on the permits. Our editorial staff quickly obtained these from Ribeiro de Araujo et al. and noted this in a brief addendum to the Acknowledgments of the paper when it was assigned to an issue. Caravaggi et al. (2021) assert that
This approach [the addendum] risks unintentionally obfuscating relevant issues and limiting the potential for review and the improvement of associated processes. We suggest, therefore that an errata [sic] would have been contextually more appropriate.
We respectfully disagree. The editorial staff and the Senior Editors discussed extensively the pros and cons of altering the Acknowledgements versus publishing an erratum. We chose the former because it was quicker to implement (permit numbers were added 12 days after the article appeared online but three months before it was assigned to an issue and paginated). Perhaps more importantly, including the permit numbers within the published paper tied them directly to the paper rather than linking them via an embedded DOI that might not be looked at or could disappear as digital technology continues to evolve. It is not at all clear how printing the permit numbers in the Acknowledgements, including the statement that they had been missed from this section when the manuscript was first posted online, and clearly stating that the addendum had been added after the version-of-record had been published, obfuscated any issues.
At the same time, however, the comments posted on Twitter and Caravaggi et al. (2021) fed into broader discussions led by the Journal of Animal Ecology and already underway across all the journals about how to best ensure that the papers we review and publish conform to current international standards for research using live animals. The BES has recently implemented a new policy on animal research ethics applicable to both lab and field studies. It is part of our broader set of Research Ethics, which also includes policies on research with human subjects and research with plants.
Adherence to these policies is being assessed by the editorial office with input from the editorial board where needed. The BES also is assembling an advisory group of Associate Editors from all its journals. This advisory group includes individuals who have expertise in animal welfare and ethics and who can advise the journal staff and Senior Editors on apparent and potential issues arising in submitted manuscripts. We are grateful to all the participants in these discussions, both within and outside of the BES, who have helped us formulate and who will help us implement this new policy.
Methods in Ecology and Evolution will continue to publish papers describing methodological advances in all areas of ecology and evolution. Some of these papers will describe methods applied to living organisms, and we will work with all our authors and our new Editorial Advisory Group to ensure that such methods are ethically sound and do not cause undue or unnecessary harm to the study organisms. We will apply these standards not only to studies involving large charismatic animals but also to any organism afforded legal protection. Local, national, and international standards for use of animals – as well as plants, fungi, and bacteria – in research continue to evolve (see, for example, Farnsworth & Rosovsky 1993, Marsh & Kenchington 2004, Drinkwater et al. 2019) and our expectations and standards for our authors, editors, manuscript reviewers and publications will evolve in tandem.