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Ready or Not, Here Comes Open Access

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Let's imagine a world without GenBank. Instead, results of the Human Genome Project and all the other genome projects have, over the years, been published intermittently on the personal homepages of the labs that did the sequencing. Some labs set up a nice little spreadsheet of their reads and made them available for download, but the formats tend to vary wildly across labs so it's tough to integrate these reads to build a larger picture. Other labs list their sequence data but, afraid of getting scooped on the analysis of it, only make it available in an image format, kind of like those websites that convert listings of email addresses to images in order to prevent spam. Still other labs keep meaning to put their reads up in some fashion, but just never seem to get around to it.

In our GenBank-free existence, there isn't much need for Blast, or most other sequence analysis tools, for that matter. It's unlikely that Katie Pollard and David Haussler would have sussed out the significance of HAR1, a gene thought to play a role in humans' cognitive differentiation from apes, or that Evan Eichler would be well known for assessing breakpoint regions in genomes and across species. After all, it would be virtually impossible to accumulate enough data in one place to perform such large-scale studies. Under these conditions, who would be motivated to write algorithms for complex analysis, anyway?

Except for the pages of this magazine, this world probably exists for you only in the nightmares you have before submitting an ambitious genomics-based grant proposal. But for advocates of open access science, this world is representative of the real-life state of scientific research today thanks to traditional models of publishing.

"Up to now … data sets [have been] stuck in laboratories or stuck in obscure corners of closed access publishers," says Matthew Cockerill, publisher of the open access BioMed Central.

"There's a direct connection between the availability of information and the availability of tools for using it," says Michael Eisen, a co-founder of the open access Public Library of Science. "Imagine if the same sort of creative power and inspiration that went into making genomic data useful" went to mining the scientific literature, he adds.

As a concept, open access is no stranger to scientists in this community. "The whole notion of true open access is something that's ingrained in the world of genomics," says Harold Varmus, also a PLoS co-founder and longtime open access supporter. Indeed, that's why genome papers have almost unconditionally gotten the unusual treatment of being fully open access across journals.

But this openness has not stretched to other kinds of data, which largely remains proprietary to individual journals. The open access movement is a push to reverse this by allowing free access to all papers, and making the research in those papers open for reuse. "The strength of science is the ability of people to look at the claims that are being made and to criticize them and to build on them," says Cameron Neylon, a lecturer at the University of Southampton and a proponent of open access. "Science works better when more people have access [to the underlying data]."

Beyond the argument that scientists should be able to build on each other's work is the far more basic concept that what the public pays for, the public should be able to access. David Solomon, a member of the Open Access Scholarly Publishing Association, puts it this way: "We're giving away what's largely paid for by public funding to publishers, who often charge large sums of money for people to access it."

Publishers, however, argue that they need to be able to make a profit, and that open access remains an unproven business model. According to Timo Hannay, publishing director at Nature Publishing Group, "We're not in a position to make everything free. The reality is, if we did that today we'd be out of business tomorrow." And nobody's looking for a situation where publishers cease to exist, because the scientific literature always has been and will continue to be a tremendously valuable resource.

Erika Linke, president of the Association of College and Research Libraries, sees open access as "trying to encourage … authors to understand that they can manage their intellectual property," she says. "There are a whole bunch of rights that an author has, and he or she can choose which of those to release to a publisher and which to retain."

Practical matters

Here's the central conundrum of the open access debate: you can't find anyone who's actually opposed to it. Really. For all the grandstanding and arguing, the fiercest opponents and supporters alike tend to support the underlying principle — that freely accessible data would be a boon to the greater scientific enterprise. In an ideal world, most everyone agrees, there would be no restrictions on scientific results. It's the real-world practical concerns that provide the point of contention.

A common practice among open access publishers is to charge authors a fee for publication, as opposed to charging readers a fee to access the paper. That's the case at PLoS, for instance, but not all publishers agree that it's a sound model. Nick Fowler, Elsevier's head of strategy, says, "We see a conflict of interest in a model where if you get published, the publisher gets paid, and if you don't get published, the publisher doesn't get paid." The model certainly does raise questions about a publisher's motivation to reject papers that might be of dubious quality, although the threat of how that might negatively affect the journal's impact factor could be seen as a hedge against such behavior. Fowler says Elsevier has no author-pays journals and doesn't plan to add any.

Another charge against the author-pays model contends that it's biased against scientists at institutions that don't have large coffers, particularly those in developing countries. Open access supporter Peter Suber says that's not the problem it seems. "Most open access publishers that charge publication fees will waive them in cases of economic hardship," he says. Open access fans say any bias exists in the traditional model as well, as scientists in developing countries or at less solvent institutions are unlikely to be able to afford subscription fees.

One of the greatest challenges for the open access movement is in gaining acceptance — perhaps interest is a better word — from mainstream scientists. In that respect, supporters can be their own worst enemies: the most vocal open access proponents can come off as zealots, their proselytizing of a new approach just a bit too strident for most people's comfort. The broader community may indeed respond favorably to a calm, rational argument, but the fact that open access has largely turned into an ideological debate has been off-putting to scientists who would rather focus on research than on the nuances of the publishing world.

Still, the movement is undeniably gaining momentum. Thanks to major institutional support, such as Harvard's policy change this year to support open access for its researchers, "it's a lot less fringey than it was," says John Wilbanks, who runs Science Commons and helps oversee Creative Commons licensing for scientific purposes.

Transition period

Traditional publishing has been around for centuries — longer, that is, than Darwin's theory of evolution. The concept of peer review is probably older than the organization you're working for and, let's face it, there may even be parts of your institution that have been developed entirely to comply with the peer review process. There are large and influential companies with a vested interest in maintaining the tried-and-true publishing model. "Scientists have a lot of respect for their journals," Varmus says. "Nobody wants to run afoul of their publishers." And one of the greatest forces in the world weighs in on the side of continuing a cycle of training and promoting scientists that has served society well as far back as we can remember. We call it inertia.

Still, a good number of traditional publishers are beginning to test the waters with open access. Nature, which still relies on its closed-access model, gets kudos from open access fans for its forays into alternatives (such as its open access EMBO journal, or the freely available Nature Precedings for pre-publication research). That's because the company is the 800-pound gorilla of scientific publishing and would risk little by ignoring the movement completely. "Nature is probably one of the only publishers that doesn't have to experiment," says Peter Suber. "It would be on the must-have list for almost every library. Nevertheless, they're experimenting. I think the reason is that they see real opportunities for advancing scholarship without sacrificing revenue."

Hindawi, a publisher based in Egypt, fully converted its titles to open access as of last year. That represents a total of 140 journals, says Paul Peters, Hindawi's head of business development. "As a smaller subscription publisher we felt that we were in a bad position to compete in the library market," he says, noting that the switch to open access was actually a move to establish a more solid business model for the company. Opening things up has been a boon to the publisher, which has seen increased submissions. Still, he says, the model is hardly steady at this point. "There's going to be a set of issues to work out" in order for open access publishing to become the norm, Peters adds. Those include settling on author charges and policies for developing countries, to name a few.

ACRL's Linke points out that it may not be possible to push the transition much faster than it's already going. Compared to how many decades the existing publisher structure has been around, the changes to accommodate open access in the past eight or 10 years constitute "a drop in the bucket" of publishing history. "It's not going to turn on a dime," she says.

Ultimately, Wilbanks says, the publishers that can make the transition will be the only ones to survive. "On the [Internet], access is a way of life. The business models have to grow up to reflect that," he says, "or we're going to see the same thing happen to the publishers that happened to the music industry."

Funding

You can't have a discussion about open access without having a discussion about funding. There's a view among scientists that open access journals are in fact more expensive — or at least more expensive personally, since they're being asked to fork over a fee for being published. The perception is often that journals are free, since institutions generally pay the costs for these rather than individual labs.

Of course, open access advocates say the money's all coming from the same place. Whether it comes from a university to pay a subscription or from a research lab to pay an author fee, the money probably started out as government funding — and virtually every penny of it came from the taxpayers' pockets. While the costs of author-pays models are not well understood on a large scale, the costs of journal subscriptions are: they're rising at rates "radically outstripping the cost of living," Wilbanks says. High-profile journals can cost a research library $20,000 or more per title every year, adds Linke. In the open access movement, the solution is simple: take the funding away from subscriptions and channel it to author fees instead.

People who study the scientific publishing world at a systems level will notice three items of interest. First, that government funding agencies control almost all of the money. Second, that university libraries control subscription agreements. And third, that the main financial beneficiaries of both the scientific results produced by grant funding and the subscription fees are the publishing firms. It would seem to be a system in which the funding agencies and libraries hold the power, and in which the publishers have the most to lose.

Proponents of open access have been delighted to see that funding agencies around the world are beginning to flex their muscles on this issue. In the US and Europe, a number of government agencies have instituted policies requiring that any grant-funded scientist  deposit his or her research into a publicly accessible database, regardless of the individual policy of whatever journal publishes it. The idea is that access for the public and for scientists gives greater impact to each dollar the government issues in funding.

Which leaves some open access fans wondering why research libraries haven't stepped up to the plate — as the argument goes, if libraries simply banded together, refusing to pay subscription fees and directing all of that money toward author fees for open access journals, traditional publishers would have no choice but to capitulate. But this ignores the incredibly awkward position libraries are in. While many library associations are staunch supporters of open access, individual libraries cannot forget that their mandate is to provide their researchers with access to the scientific literature. And no matter how much they might want to take a stand, it would go against their raison d'être. "It's a balancing act," says Linke at ACRL.

The long view

The goal of some open access publishers has been to out-Nature Nature: build a successful empire of highly selective journals with respectable impact factors, and convince scientists to publish with them on traditional publishing merits rather than on the basis of being open access. There's a problem with this goal. The truth of scientific publishing is this: the cost to produce a journal rises in lock step with its success. In a journal like Nature, with its nearly 95 percent rejection rate, studies estimate that it costs more than $10,000 — even as much as $30,000 — to publish each paper. A significant chunk of that cost goes toward paying editors to oversee the peer review process, which must be performed on far more papers than are actually published. An equally selective open access journal that relies on author fees in the neighborhood of $3,000 per published paper simply can't make the math work out. It's not possible to break even, let alone make a profit, in those conditions.

Journals that are less selective cost significantly less to produce. PLoS, for example, has shored up its revenue base by publishing a suite of journals with lower rejection rates, as well as its experimental online journal PLoS One (see PLoS description below), that bring in enough revenue to pick up much of the financial slack for the high-end titles. To many detractors, this is a fundamental failing of the open access model: that it can only survive when publishing mediocre-quality journals.

The plan to bring open access publishing to scientists' attention in this way — fighting traditional publishers on their own turf — misses the point of the open access vision. If your options are running a fleet of mediocre journals or publishing a high-quality but ultimately unsustainable journal, you've failed from the start. What will make open access both viable and successful is the game-changing model that champions like Harold Varmus and Michael Eisen have dreamed of from the beginning: a completely new approach to publishing that separates the instance of publication from the process of peer validation.

That's the vision behind PLoS One, a model that says any paper, so long as it's methodologically sound, should be made available to the community. And then it's up to scientists to read the paper and weigh in on it — an after-the-fact peer review — by embracing social networking, ranking, commenting, and the many other advances of a Web 2.0 world. Papers that are ranked highly will float to the top, just as the most interesting news articles bubble up with tools like Digg or the most-viewed list on news websites. The question for researchers changes from 'which papers should be published?' to 'which of the published papers are worth reading?' It is in this context that scientists can at last begin to perform the sort of sweeping analysis of the literature that many a researcher has wished for during an experiment (wouldn't it be nice to filter all the results published on this gene or protein?) but set aside as mere fantasy. "If you're going to do innovative things with content," says Wilbanks at Creative Commons, "the content has to be legally available."

Perhaps the greatest challenge to this model is resistance from a scientific community that has been raised with the idea that if something is published it must be worthy. That's not the mindset of the Internet-based world, where it's commonly accepted that anyone can put anything out there, and it's up to good Web citizens to help alert others to what's worth reading and what's not.

The most difficult step for scientists in the rise of open access may be accepting someone else's right to publish a thoroughly awful paper, and to trust that community response will make sure that such a paper is properly discredited, in return for the right to gain free access to all of the truly meritorious research.

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Open Access: what does it all mean?

Open access: The pure form of open access is considered research that's made freely available for reuse in any way another scientist might dream up. In general, as long as the original author is credited for what's his, any other scientist can add to the work with no strings attached.

Public access: By contrast, public access usually describes repositories like PubMed Central, where papers may be made available but can still be subject to various copyright barriers, or may not contain the full article content. Public access can also mean papers are available in locked formats like PDF, preventing them from being mined or analyzed.

Key players: Among open access publishers, some of the largest or best known are BioMed Central (just acquired by Springer), Hindawi, Medknow, and the Public Library of Science. Central organizations in the space include SPARC, an advocacy group for public access, and Creative Commons, which provides access-friendly licensing options for publishers. The Open Access Scholarly Publishing Association is a newly formed group to lobby for full open access.

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Reluctant Publishers and the Birth of PLoS

Pat Brown, Michael Eisen, and Harold Varmus have become the face of the Public Library of Science, but none of them ever set out to be a publisher.

Eisen was a postdoc in Brown's lab at Stanford when he first realized that access was even an issue. It was the early days of microarrays, and Brown's team was using computers to tackle some of the original high-throughput problems in biology. "One of the things we thought about doing was to go out and mine the literature — pull out all the papers that mention genes that are upregulated in this condition," Eisen recalls. "It seemed like a natural thing to do to get the contents of those papers and suck them into a computer and do interesting and cool stuff with it."

But when they went to Stanford's library with the request, they were turned down. "It was the first moment I thought about what it meant, the fact that the scientific literature was owned by publishers," Eisen says.

In 2001, Brown and Eisen kicked off a petition — an online initiative scientists would sign to indicate their support for free access to the literature and their commitment to publish only in open access venues. Thousands of researchers signed the petition. But "a lot of people are supportive right up to the point where it comes to where they're going to submit their paper," says open access advocate Cameron Neylon. "People are coming up for tenure review or promotion review, they want those 10 papers in those recognized journals." The petition failed to give open access the widespread support that Eisen and Brown had envisioned; scientists kept publishing in traditional journals regardless of access policies.

By 2003, they realized they would need to take a different tack. Joined by Varmus, they launched PLoS with the goal "to create a bunch of … high-profile, high-end journals that would convince people that high quality and open access could be synonymous," Eisen says. They raised $13 million in grant support from the Gordon and Betty Moore Foundation and other philanthropies and opened PLoS Biology.

Traditional publishers have had a field day with PLoS, arguing that the need for grant funding served as proof of their own argument that open access was not a viable business model. But today, Eisen says that PLoS as a whole is near the break-even point, with enough journals making a profit to support the journals that aren't. "The fact that we now have multiple journals that are actually profitable is a huge thing for convincing others that open access is a viable option," Eisen says. The funny thing, he notes, is that their success in getting high-profile journals started means scientists who publish ther often are completely unaware of the access difference.

PLoS again made headlines when it launched PLoS One, an online venue that has a completely different approach. Papers are reviewed simply for sound methodology, and the peer-review process becomes a community effort that takes place when the paper comes out using commentary, rankings, and other Web 2.0 tools. This idea is "much closer to what our initial ambition was," Eisen says. Publish quickly, and then let scientists weigh in, rather than holding up access to the research for months of behind-the-doors peer review. "This is getting us close to the point where we've always wanted to be," he adds.

Next up is a task for the community: developing the "killer apps" that will be to the literature what Blast has been for sequence data. In Eisen's vision, that might mean that "when you're doing an experiment, even as you're collecting your data, it's connecting your data" to previously published results.

The ultimate irony to Eisen is that he is now a part of the system he spent years fighting. "What was initially really inspired by a desire to basically break apart the whole way publishing was done has led us to spend six years as publishers," he says.

"A lot of what motivates us now is just the frustration and anger that when people publish papers that are funded by the government, that everybody in the world can't read it," he adds. "That's an absurdity."

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PubMed Central: The 'Mildly Destabilizing' Compromise

PubMed Central has become a critical component of the scientific research landscape, but 10 years ago it was just a gleam in Harold Varmus's eye. Originally conceived as E-Biomed, the vision was far more broad-reaching than what eventually became PubMed. "The original idea for PubMed Central was probably too radical," Varmus says. "I probably went too far initially."

'Too far' was a scheme for a completely new system where articles could be submitted to a central database prior to publication so that scientists could get earlier access to fresh research. Their apparent replacement put publishers in an uproar, and they mounted what Varmus remembers as "massive resistance" to the concept. In the spirit of not letting the perfect be the enemy of the good, Varmus's vision for E-Biomed was pared back to what would eventually become PubMed Central, which allowed but did not require publishers to deposit papers. Michael Eisen says while the database began as a compromise, it served a valuable purpose of being "mildly destabilizing" to the existing culture.

Today, more than 400 journals contribute to PubMed — a success that feeds information about some 650,000 articles daily to users. Still, many of those articles are not full text, and their use for large-scale analysis is limited. A few years ago, the US Congress called for making NIH-funded articles available in PubMed; again, resistance from publishers led to the policy being voluntary rather than mandatory. But that led to an abysmal participation rate of about 5 percent, says David Lipman, director of the National Center for Biotechnology Information at NIH. This year, Congress changed the policy to require scientists to deposit NIH-funded papers in PubMed within 12 months of publication. Similar policies have been implemented in the UK and elsewhere, some with shorter time frames for submission. There are hopes that NIH will move to a six-month policy to get research out there faster.

But the battles continue, and there's a bill in Congress now attempting to overturn the public access policy. In September, 33 Nobel laureates signed a letter supporting the access policy and opposing the bill. "The scientific literature is our communal heritage," they wrote. "The NIH came through with an enlightened policy that serves the best interest of science, the scientists who practice it, the students who read about it, and the taxpayers who pay for it."

Open access fan Peter Suber says the bill is "a sign that publishers are not giving up. … The challenge is to get them to a point where they will choose to adapt rather than fight."

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Many Flavors of Open Access

When people refer to open access journals, there are actually a number of different models that they have in mind. Nick Fowler, head of strategy at Elsevier, breaks them down into the four main flavors.

Author pays BioMed Central and PLoS both utilize this approach, which relies on authors paying a fee to be published and then not having subscription charges for anyone to access the journal. Fowler says that about 1 percent of all articles are published in author-pays journals, and that that number has remained consistent for the past five years or so.

Sponsored articles

This is a hybrid model, based primarily on subscription fees, in which authors are asked after publication whether they're interested in paying a fee to sponsor the article, thereby making it freely available to the community. According to Fowler, only about one in 1,000 authors generally pays the fee to sponsor an article. But more institutions are beginning to take advantage of this concept. Wellcome Trust and Howard Hughes Medical Institute, for instance, both have negotiated deals with Elsevier in which they pay the fee to sponsor articles authored by their researchers.

Delayed access

This is the model used by Elsevier's Cell, among other journals. Publishers using the delayed access approach keep literature behind closed doors for a certain period of time — often 12 months — and then make it freely available through a website. In life sciences, Fowler says, research moves so rapidly that releasing papers after a year doesn't carry the threat of cancelled subscriptions, so more publishers are willing to try this.

Archiving

Also known as public access, this approach means that papers are deposited in some kind of central repository such as PubMed. Often the manuscript being archived doesn't exactly match what appears in the journal; it have errors or omissions, Fowler says. This model is being used more and more as funding agencies introduce policies requiring that the research they're making possible is made freely available within six months or a year.

An Acquisition, an Association, and a Celebration

Peter Suber knows better than anyone that the flow of open access news has gone from a weak flow to a firehose-like level. Suber, who writes the online newsletter Open Access News on behalf of access advocacy group SPARC, has gone from occasional updates to as many as 10 or 15 news items per day in his quest to keep readers posted.

In the past month alone, the movement for open access saw a number of milestones. For starters, the group celebrated its first holiday — Open Access Day was held on October 14, with a number of organizations taking note of the occasion. Community bloggers made a special effort to raise awareness for the concept, releasing essays, videos, and other materials to introduce unfamiliar scientists to it.

The day was also marked by the launch of a new professional association that aims to establish standards and best practices for open access publishing. The Open Access Scholarly Publishing Association includes as founding members BioMed Central, Hindawi, PLoS, SPARC Europe, and others. "Open access has reached the point where it's time to have a professional organization," says David Solomon at Michigan State University, who helped launch the association. The goal is to advocate for open access journals while making sure that publishers who claim to be open access are adhering to good practices, such as ensuring full accessibility to content, not spamming readers or potential readers, having full disclosure about charges associated with publishing, and so forth. "To be a member of the organization we all agree that it has to be immediate, full open access," Solomon says.

And in what may prove to be the most momentous event of all, open access got a serious credibility boost when publishing giant Springer acquired BioMed Central, a publishing company founded by Vitek Tracz in 2000 with an open access charter for all of its journals. At the time of its sale, BioMed Central was publishing more than 180 peer-reviewed journals, including Genome Biology and BMC Bioinformatics, and had annual revenues of approximately €15 million.

Advocates believe this is a significant vote of confidence in the movement — a can't-be-ignored deal that legitimizes the very business model traditional publishers have been so quick to dismiss. Matthew Cockerill, publisher of BMC, says that his company "has certainly proven the open access business model to be viable." But only time will tell whether it winds up being a turning point for the field or just another incremental step in a slow transition process.