by Laura Luebbert and Lior Pachter

Background (by LL)

Four years ago, during the first year of my PhD at Caltech, I participated in a journal club organized by the lab I was rotating in. I was assigned two classic papers on the honeybee waggle dance: “Visually Mediated Odometry in Honeybees”  (Srinivasan et al., JEB 1997)1 and “Honeybee Navigation: Nature and Calibration of the ‘Odometer’” (Srinivasan et al., Science 2000)2. Since I was not familiar with honeybee behavior, I decided to expand my literature review to other papers on the topic, including “Honeybee Navigation En Route to the Goal: Visual Flight Control and Odometry”  (Srinivasan et al., JEB 1996)3 and “How honeybees make grazing landings on flat surfaces” (Srinivasan et al., Biological Cybernetics 2000)4. While reading these papers, I sensed something strange; I had the feeling that I was looking at the same data over and over again.

I decided to examine the figures and results in the papers carefully, and upon further examination,  I found inconsistencies in the results and instances of identical data being reported for different experiments in distinct papers. I was deeply concerned by these findings and presented them at the journal club meeting using animations and overlays to show that the data was indeed identical; the original slides from my journal club presentation on April 9, 2020 are shown below for one example of identical data reported for different experimental conditions and replicate numbers in (Srinivasan et al., JEB 1997)1.

I had imagined that the response to my presentation would be concern and advice on how to report my findings. Instead, both within and outside of Caltech, the response amounted to little more than a collective shrug.

My rotation advisor, a tenured professor, told me that they did not know what to do, so I turned to the instructor of a class I had just finished on “Responsible Conduct of Research”—a required class for first-year PhD students at Caltech. They told me that “it is a question of how you want to spend your time” and “a lot of the scientific literature has problems […], science is an imperfect process”. What was an aspiring scientist supposed to take away from this? I had assumed that ensuring scientific integrity would be a top priority for scientists, not an afterthought. 

Eventually, on May 28, 2020, I took my frustrations to Twitter, hoping that someone would follow up on my discovery. After help from Dr. Elisabeth Bik, I ended up posting two PubPeer articles, available here and here. However, both posts have been ignored by journal editors and authors for the past four years. 

I was thinking about the collective silence that afflicts scientists when uncomfortable allegations of misconduct are brought forth when, earlier this year, Bill Ackman’s plagiarism accusations against Prof. Claudine Gay were seized upon not only by academics but the public at large. Why is it that accusations of misconduct against men are routinely dismissed as inconsequential while a high-standing female academic missing citations for sub-sentences in the methods and acknowledgments of her PhD thesis is worthy of a New York Times article?

As I regained some faith in scientific integrity, I decided to revisit the honeybee waggle dance papers, and I ended up writing a detailed report in collaboration with my advisor, Lior Pachter. The report, titled “The miscalibration of the honeybee odometer” is now posted on the arXiv. We discuss its implications below.

The miscalibration of the honeybee odometer (by LL and LP)

After reading several papers on honeybee navigation coauthored by Srinivasan, we determined that there were numerous instances of apparent misconduct in addition to the cases of data duplication first presented by Laura in the journal club four years ago. In our report, we discuss numerous papers published over the course of a decade, that are part of the foundation of the field of honeybee behavior, and continue to be cited today. We provide clear evidence that several of these papers contained erroneous information, and many of them contain duplicated and manipulated data. Importantly, the report became a critique not of a single paper, but of a large body of work. We decided it was of the utmost importance for researchers working on honeybee navigation to learn that classic experiments on which the field was based ought to be repeated to verify that the claims made are correct. However, we soon found that there was no medium to publish our manuscript.

We started with bioRxiv, which promptly rejected the manuscript on screening, telling us that we should “reformat it as a research paper presenting new results along with appropriate methods used, rather than simply a critique of existing literature.” Moreover, we were told that our manuscript contained “content with ad hominem attacks,” even though it was merely a factual report of the issues we observed with appropriate citations of the affected papers, with no attack on any people or specific persons.

Faced with rejection from bioRxiv, we decided to submit the manuscript to the Journal of Experimental Biology (JEB), which had published several of the problematic papers. JEB rejected our manuscript for publication but told us they were “investigating the issues raised.” They also said that they “can only investigate issues on papers published in our journals, so you will also need to contact individually each of the other journals that published the papers with which you have concerns.” (Note the use of the word “you“, which we interpreted as an abdication of responsibility by the journal to ensure scientific integrity at large.) Again, we found ourselves without a venue in which to describe problematic results across several papers. We also felt that contacting individual journals for corrections would not serve the community well. Our point was about an entire body of work, not nitpicks regarding individual articles. 

The importance of reporting the problems at large across papers is exemplified by the Expressions of Concern published by JEB on June 25, 2024, in response to our manuscript submission to their journal, which can be found here and here. In their Expressions of Concern, JEB states that “the 1996 paper is likely to contain the correct values of the width of the narrow tunnel (11 cm)”, “It appears that Fig. 7 does not contain the correct graph for the searching distribution with the landmark positioned at Unit 9,” and “M. V. Srinivasan believes that the length of the tunnel was not 3.35 m as reported in the 1996 paper, but 3.20 m as indicated in Srinivasan et al. (1997).” Readers are supposed to rest assured that these “issues do not alter the overall results and conclusions of the paper.” We were surprised that the bar for publication at JEB is “belief” and that results are only “likely” to be correct.

Perhaps, if the issues in the two JEB papers were the only issues with this body of work, one could excuse them as human error—which should still cast doubt on the conclusions of the paper. However, JEB was made aware of the issues with this body of work at large, which includes many more instances of data duplication and apparent manipulation across a total of six papers (as far as we found), yet JEB still decided to dismiss their occurrence in their papers. JEB stated in their Expressions of Concern that they “are publishing this Expression of Concern to make readers aware of the issues and our efforts to resolve them,” though no such efforts are described in either Expression, and readers are misled by JEB’s failure to mention that these are not isolated instances pertaining only to the two papers in question. We found the response from “the leading primary research journal in comparative physiology” to be disappointing.

We finally submitted our manuscript to the arXiv, where it was published after being placed on hold for two weeks without any explanation. All of our findings regarding the scientific misconduct in honeybee papers are described in detail here5: https://arxiv.org/pdf/2405.12998 Notably, JEB failed to cite our arXiv manuscript in their Expressions of Concern (our manuscript appeared on May 8, 2024—over a month before their Expressions) and instead mentions only the limited PubPeer articles from 2020, which they had ignored for four years.

Leaving aside the specifics of honeybee, our experience with correcting the literature made us realize that there seems to be no venue right now for critiquing a body of work by an author. Comments on PubPeer are great; and corrections or retractions in journals are useful, but neither serve to alert a community to problematic behavior across numerous articles by an author. We think that our paper would have benefitted from peer review and a mechanism for commentary. For the latter, we decided to write this blog post. For the former, we suggest a Journal of Scientific Integrity.

References

1. Srinivasan, M., Zhang, S. & Bidwell, N. Visually mediated odometry in honeybees. J. Exp. Biol. 200, 2513–2522 (1997).

2. Srinivasan, M. V., Zhang, S., Altwein, M. & Tautz, J. Honeybee navigation: nature and calibration of the ‘odometer’. Science vol. 287 851–853 (2000).

3. Srinivasan, M., Zhang, S., Lehrer, M. & Collett, T. Honeybee navigation en route to the goal: visual flight control and odometry. J. Exp. Biol. 199, 237–244 (1996). [article currently removed from journal website, so the link is to PubMed]

4. Srinivasan, M. V., Zhang, S. W., Chahl, J. S., Barth, E. & Venkatesh, S. How honeybees make grazing landings on flat surfaces. Biol. Cybern. 83, 171–183 (2000).

5. Luebbert, L. & Pachter, L. The miscalibration of the honeybee odometer. arXiv [q-bio.OT] (2024).