Scientists are becoming increasingly frustrated by how long it seems to take to publish papers. But is it really getting worse? THE WAITING GAME BY KENDALL POWELL 148 | NATURE | VOL 530 | 11 FEBRUARY 2016 © 2016 Macmillan Publishers Limited. All rights reserved FEATURE NEWS hen Danielle Fraser first indexed in the PubMed database that had listed preprint model to accelerate publishing. “We submitted her paper for submission and acceptance dates (see go.nature. need a fundamental rethinking of how we do publication, she had little com/zjdqhn). His study, done for Nature, this,” Vosshall says. idea of the painful saga that found no evidence for lengthening delays2: lay ahead. the median review time — the time between THE PITCH She had spent some submission and acceptance of a paper — has In March 2012, Stephen Royle, a cell biologist 18 months studying thousands hovered at around 100 days for more than 30 at the University of Warwick, UK, started on W of fossil species spread across years (see ‘Paper wait’). But the analysis comes a publication mission of his own. His latest North America from the past 36 million years, with major caveats. Not all journals — includ- work answered a controversial question about and now she had an intriguing result: animal ing some high-profile ones — deposit such how cells sense that chromosomes are lined populations were spread widest across lati- time-stamp data in PubMed, and some jour- up before dividing, so he first sent it to Nature tudes in warm, wet climates. Her work, crucial nals show when a paper was resubmitted, rather Cell Biology (NCB), because it is a top journal to earning her PhD at Carleton University in in his field and an editor there had suggested Ottawa, Canada, might be used to make predic- he send it after hearing Royle give a talk. It tions about the response of mammals to climate was rejected without review. Next, he sent it to change — a key question in ecology today. So, “It takes forever Developmental Cell. Rejected. His next stop, the with her PhD adviser’s encouragement, she sent Journal of Cell Biology, sent the paper out for it to Science in October 2012. to get the work review. It came back with a long list of necessary Ten days later, the paper was rejected with revisions — and a rejection. a form letter. She sent it to another prestig- out, regardless Royle and his lab spent almost six months ious journal, the Proceedings of the National doing the suggested experiments and revis- Academy of Sciences. Rejected. Next, she tried of the journal.” ing the paper. Then he submitted the updated Ecology Letters. Bounced. “At this point, I manuscript to Current Biology. Rejected. EMBO definitely was frustrated. I hadn’t even been than submitted for the first time. “Resetting the Journal. Reviewed and rejected. reviewed and I would’ve loved to know how to clock is an especially pernicious issue,” Him- Finally, in December 2012, he submitted it to improve the paper,” recalls Fraser. “I thought, melstein says, and it means that the analysis the Journal of Cell Science (JCS), where it was ‘Let’s just get it out and go to a journal that will might be underestimating publication delays. reviewed. One reviewer mentioned that they assess the paper’.” Some data suggest that wait times have had already assessed it at another journal and In May 2013, she submitted the paper to increased within certain subsets of journals, thought that it should have been published Proceedings of the Royal Society B, considered such as popular open-access ones and some then. They wrote that the work was “beauti- a high-impact journal in her field. The journal of the most sought-after titles. At Nature, the fully conducted, well controlled, and conserva- sent it out for review — seven months after her median review time has grown from 85 days tively interpreted”. A second reviewer said that initial submission to Science. “Finally!” Fraser to just above 150 days over the past decade, it should not be published. The editor at JCS thought. What she didn’t know was that she had according to Himmelstein’s analysis, and at decided to accept it. The time between first sub- taken only the first steps down the long, bumpy PLoS ONE it has risen from 37 to 125 days over mission to Nature Cell Biology and acceptance road to publication: it would take another roughly the same period. at JCS was 317 days. It appeared online another three submissions, two rejections, two rounds Many scientists find this odd, because they 53 days later3. The work went on to win the JCS of major revisions and numerous drafts before expect advances in digital publishing and the prize as the journal’s top paper for 2013. the paper would finally appear. By that point, proliferation of journals to have sped things up. Despite the accolade, Royle says that the she could hardly bear to look at it. They say that journals are taking too long to multiple rejections were demoralizing for his Fraser’s frustration is widely shared: research- review papers and that reviewers are request- student, who had done the experiments and ers are increasingly questioning the time it takes ing more data, revisions and new experiments needed the paper to graduate. He also thinks to publish their work. Many say that they feel than they used to. “We are demanding more and that the paper deserved the greater exposure trapped in a cycle of submission, rejection, more unreasonable things from each other,” says that comes from publication in a more prestig- review, re-review and re-re-review that seems Vosshall. Journal editors counter that science ious journal. “Unfortunately, the climate at the to eat up months of their lives, interfere with job, itself has become more data-rich, that they work moment is that if papers aren’t in those very top grant and tenure applications and slow down to uphold high editorial and peer-review stand- journals, they get overlooked easily,” he says. the dissemination of results. In 2012, Leslie ards and that some are dealing with increasing And Royle, who has done several publication- Vosshall, a neuroscientist at the Rockefeller numbers of papers. They also say that they are time analyses and blogged about what he found, University in New York City, wrote a commen- taking steps to expedite the process. has shown that this experience is not unusual. tary that lamented the “glacial pace” of scientific Publication practices and waiting times When he looked at the 28 papers that his lab had publishing1. “In the past three years, if anything, also vary widely by discipline — with social published in the previous 12 years, the average it’s gotten substantially worse,” she says now. “It sciences being notoriously slow. In physics, the time to gestate from first submission to publi- takes forever to get the work out, regardless of pressure to publish fast is reduced because of cation was the same as a human baby — about the journal. It just takes far too long.” the common practice of publishing preprints 9 months (see go.nature.com/79h2n3). But is the publication process actually — early versions of a paper before peer review But how much of these delays were his own becoming longer — and, if so, then why? To find — on the arXiv server. Some of the loudest doing? To publish the chromosome paper, out, Nature examined some recent analyses on complaints about publication delays come Royle indulged in the all-too-familiar practice time to publication — many of them performed from those in biological fields, in which com- of journal shopping: submitting first to the most by researchers waiting for their own work to see petition is fierce and publishing in prestigious prestigious journals in his field (often those with the light of day — and spoke to scientists and journals can be required for career advance- the highest impact factor) and then working his editors about their experiences. ment. This month, a group of more than 70 sci- way down the hierarchy. (Nature Cell Biology’s The results contain some surprises. Daniel entists, funders, journal editors and publishers current impact factor is 19; JCS’s is 5.) Journal Himmelstein, a computational-biology are meeting at the Howard Hughes Medical impact factor or reputation are widely used by graduate student at the University of Cali- Institute campus in Chevy Chase, Maryland, scientists and grant-review and hiring commit- ILLUSTRATION BY MATT MURPHY MATT BY ILLUSTRATION fornia, San Francisco, analysed all the papers to discuss whether biologists should adopt the tees as a proxy for the quality of the paper. On 11 FEBRUARY 2016 | VOL 530 | NATURE | 149 © 2016 Macmillan Publishers Limited. All rights reserved NEWS FEATURE Some scientists complain that publishing papers takes too long, PAPE WAIT but data show a complex picture. EVIEW TIME PODUCTION TIME An analysis of all papers in PubMed up to 2015 with listed submission and The same analysis of Pubmed papers suggests that the time between acceptance acceptance dates suggests that the median time from submission to acceptance and publication has dropped, probably because technology has improved. has hovered at around 100 days, although it has gone up at some journals. 75 200 A few journals with quick review times started in 150 50 2000, lowering the median. 100 25 50 1980: 4,353 journals 2015: 9,045 journals in the PubMed database. in the PubMed database. to publication (days) to acceptance (days) 0 0 Median time from acceptance Median time from 1980 1990 2000 2010 2000 2005 2010 2015 Median time from submission Median time from Date accepted Date published online 5 REF.