The Tao of Open Science for Ecology

The field of ecology is poised to take advantage of emerging technologies that facilitate the gathering, analyzing, and sharing of data, methods, and results. The concept of transparency at all stages of the research process, coupled with free and open access to data, code, and papers, constitutes "open science." Despite the many benefits of an open approach to science, a number of barriers to entry exist that may prevent researchers from embracing openness in their own PeerJ PrePrints | http://dx.doi.org/10.7287/peerj.preprints.549v1 | CC-BY 4.0 Open Access | rec: 21 Oct 2014, publ: 21 Oct 2014 P re P rin ts


INTRODUCTION
Ecology stands at the threshold of a potentially profound change.Ever-increasing computational power, coupled with advances in Internet technologies and tools, are together catalyzing new ways of pursuing ecological investigations.These emerging approaches facilitate greater communication, cooperation, collaboration, and sharing, not only of results, but also of data, analytical and modeling code, and potentially even fully documented workflows of the processes-warts and all-that lead to scientific insights.This vision of free and unfettered access to all stages of the scientific endeavor has been called ''open science'' (Nielsen 2011).As an integrative and highly multidisciplinary field, ecology particularly stands to benefit from this open science revolution, and many ecologists have expressed interest in enhancing the openness of ecology.To date, such conversations among ecologists have largely occurred online (e.g., discussed in Darling et al. 2013); thus it seems timely to present an introduction and path (Tao) to open science for ecologists who may or may not currently be active in the social media forums where the discussion is evolving.We give an overview of the rise of open science, the changes in mindset that open science requires, and the digital tools that can enable ecologists to put the open science mindset into practice.
The exchange of scientific information was institutionalized in the 1660s with the establishment of the Philosophical Transactions of the Royal Society of London and the Journal des Sçavans, the first scientific journals (Beaver and Rosen 1978).While these journals provided platforms for scientists to share their results and ideas, they were largely accessible only to elitesthose who could afford a subscription themselves, or those who belonged to an institution that held copies (Nielsen 2011).Individual scientists (i.e., single authors) published in these journals to establish precedence of discovery; the notion of collaboration among scientists does not seem to have taken hold until the 1800s (Beaver and Rosen 1978).
The scientific world looks very different now.Advances in computing power and speed have accelerated not only individual scientists' discoveries but also their collaborative potential (Box 1).
Modern scientists constitute a global college, its philosophical transactions enabled by the Internet (Wagner 2008), and collaboration has become the predominant norm for high-impact research (Wu ¨chty et al. 2007).Technological developments also have enabled the capture (at ever increasing rates) of a previously unimaginable volume of data and metadata (Reichman et al. 2011, Dietze et al. 2013), and have underlain the use of increasingly complex models and analysis techniques to understand these data.Traditional paper notebooks cannot meet the challenges of these new rates of accumulation, sharing, and recombination of ideas, research logs, data, and analyses (Ince et al. 2012, Strasser andHampton 2012).The tools and approaches that together constitute open science can help ecologists to meet these challenges, by amplifying opportunities for collaboration and rewarding the creation of the consistent and machine-readable documentation that is necessary for reproducibility of complex projects.
While interest in this new paradigm is on the rise (Fig. 1), it must be acknowledged that both technical and sociocultural obstacles impede adoption for some ecologists.For example, precedence, attribution, investment, and payoff are high-stakes issues for professional scientists (Hackett 2005).Adopting open practices means ceding some control of these issues, learning new standards and practices for exerting control over others, and devoting precious time to revising familiar modes of research and communication in a seemingly foreign language (Box 2).Yet hewing to traditional practices carries its own risks for the individual investigator.Errors and oversights can persist far longer when experimental design, raw data, and data analysis are held in private; even once published, weeks and months can be wasted in chasing reproduction of results because methods are documented only as fully as a journal word count permits; labs can become isolated, their advancement slowed, for lack of substantive interaction with others.As has been demonstrated in other disciplines, open science can help to mitigate these risks, to the immediate benefit of the individual practitioner (Lawrence 2001, Davis andFromerth 2007).A community can help the individual scientist identify pre-publication errors, before they result in paper retractions, damaged reputations, and scientific backtracking.
Moreover, open science promises many longer term benefits to the scientific community.The adoption of standard best practices and cultural norms for public archiving of data and code will advance discovery and promote fairness in attribution.The use of open-source tools and open-access data and journals will help to further democratize science, diversifying perspectives and knowledge by promoting broader access for scientists in developing countries and at under-resourced institutions, fostering the citizen science that is already a major source of data in some ecological sub-disciplines (Cooper et al. 2014), and improving the communication of scientific findings both to the general public (Fausto et al. 2012) and to the non-governmental organizations, managers, and policymakers tasked with putting science into practice.
Here, we discuss the changes in mindset and the tools that can help interested ecologists to find the path toward practicing open science themselves, to facilitate its practice by their students and other colleagues, or both.

Data stewardship, not data ownership
Traditional views on data ownership hold that data are proprietary products of the researcher Box 1

Technological advances driven by scientists
Every scientist now uses the Internet, but few are aware of how the Internet grew out of a highly collaborative and open process involving development of publicly available and commentable standard protocols (http://www.fcc.gov/openinternet;Cerf 2002).The availability of ''open source'' software (a term first coined in the 1990s) radically democratized and expanded participation in the Internet community in the late 1980s-early 1990s.''Open source'' encompasses not only compilers and applications but also protocols and specifications such as the domain name system (DNS) that allows pinpointing specific networked computers (''hosts'') around the world, and HTTP/HTML specifications that provide the basis for the World Wide Web.
Members of the scientific research community were early recipients of these advantages, with the National Science Foundation supporting and nurturing growth of the Internet-based NSFNET from roughly 1985-1995(National Science Foundation 2007).In that era, it was scientists who were largely communicating through the Internet (gopher, email), transferring their data (FTP), and running analyses on remote servers (telnet, shell access, X11), often with privileged access to fast networks and accounts on powerful computational servers.Within this computer savvy community, ''power users'' leveraged the Internet most effectively via learning computational skills that were largely command-line based.The legendary, free GNU suite of software was standard issue for many computers joining the Internet in the late 1980s, and made that early generation of networked ''scientific workstations'' (from Sun, SGI, DEC, or NeXT) the sought-after systems of their day.
These early forays into powerful software helped birth the plethora of tools now available to the modern scientist.Today, free, multi-platform, open source tools from the Linux Foundation (free operating system), the Apache Software Foundation (free Web server), the Mozilla Foundation (free Web, email, and other applications), the PostgreSQL Global Development Group (free enterprise database), the Python Software Foundation (free programming language), and the R Foundation for Statistical Computing (analysis and statistical language) are enabling researchers across the globe to dialog with one another via cutting edge communication, execute powerful data manipulation, and develop community-vetted modeling and analysis tools at minimal individual cost.

Box 2
A glossary of open science for ecologists citizen science: enabling interested citizens to contribute their time, observations, and expertise to assist and inform the scientific research process; may be an aspect of crowd-sourcing.
code repository: an accessible, central place where computer code is stored to facilitate the collection, manipulation, analysis, or display of data.
crowd-sourcing: leveraging the expertise and participation of many individuals, to provide more perspectives, critiques, data contributions, code contributions, etc. to advance a (scientific) process.
data life-cycle: the pathway researchers trace when confronting a challenge with data, from idea generation through to making observations and drawing inference.Popularly dissected into eight intergrading phases: Plan, Collect, Assure, Describe, Preserve, Discover, Integrate, Analyze (Michener and Jones 2012).
data management: the development and execution of architectures, policies, practices and procedures that properly manage the full data life-cycle needs of an enterprise (Mosley et al. 2009).
data repository: an accessible, central place where accumulated files containing collected information are permanently stored; typically these house multiple sets of databases and/or files.
open access: providing free and unrestricted access to research products, especially journal articles and white papers-to be read, downloaded, distributed, reanalyzed, or used for any other legal purposewhile affording authors control over the integrity of their work and the right to be acknowledged and cited (adapted from the Budapest Open Access Initiative definition, Chan et al. 2002).
open data: data that can be freely used, reused, and redistributed without restrictions beyond a requirement for attribution and share-alike (Molloy 2011).
open source: computer code (software) that is available for free distribution and re-use, with source code unobscured, and explicit acknowledgement of the right to create derived works by modifying the code (Gacek and Arief 2004).
open science: the idea that scientific knowledge-including data, observational and experimental design and methods, analytical and modeling code, as well as results and interpretations of these (e.g., as reported in publications)-can and should be made freely accessible to anyone, and represented in transparent and reusable formats as early as practical in the discovery process, by preprint: a draft version of a paper distributed (usually in an online repository such as arXiv) before a final, peer-reviewed journal or reporting agency has accepted or formally published the paper (Desjardins-Proulx et al. 2013).
provenance: the origin of data, including any transformations occurring along the way.reproducibility, replicability, and repeatability: while formal definitions of these terms vary widely and across disciplines, these all point to a hallmark of science, which is the ability to repeatedly generate or observe outcomes consistent with scientific understanding, based on explicit specification of theories, models, and methods, and their expected material realizations or outcomes.This concept prescribes a need for sufficient access to data and analytical code to verify that a purported result is valid, as well as to examine these for errors and biases (Peng 2009, Stodden 2009, Jasny et al. 2011, Stodden et al. 2013;but note Drummond 2009 andCasadevall andFang 2010 use somewhat different definitions).
transparency: sufficiently detailed description of a scientific process to enable meaningful public scrutiny and examination, with nothing intentionally obscured by technology or process.
version control: a system that manages snapshots (and hence ''revisions'' or ''versioning'') of code and data for a project (Wilson et al. 2014).Facilitates detailed documentation to enable tracing any significant changes over a project's lifetime.(Sieber 1989).By definition, this data-ownership mindset limits the potential for data sharing as a given researcher can restrict the conditions and circumstances by which their data are dissemi-nated.These views have persisted for a variety of reasons (Sieber 1989, Hampton et al. 2013, Lindenmayer and Likens 2013) and ecologists historically have treated data as proprietary, v www.esajournals.orgwhether or not the data collection has been funded by taxpayers and might reasonably be considered public property (Obama 2013).
Under the principles of open science, data are generated with the expectation of unfettered public dissemination.This fundamental shift in thinking from ''I own the data'' to ''I collect and share the data on behalf of the scientific community and society'' is essential to the transparency and reproducibility of the open science framework.When data are available, discoverable, reproducible, and well-described, scientists can avoid ''reinventing the wheel'' and instead build directly on those products to innovate.For example, authors' reluctance to submit null results for publication leads to a ''filedrawer'' effect that can not only systematically bias the published literature (Iyengar andGreenhouse 1988, Franco et al. 2014), but also allows independent scientists to go repeatedly down the same blind alleys.Structures to store, share, and integrate data contribute to preventing such waste of scientific and public resources.Beyond this greater efficiency, data sharing also contributes to the production of entirely new scientific products that were not envisioned at the time data were collected (Hackett et al. 2008, Carpenter et al. 2009).
Norms have yet to be established in ecology for how soon after collection data should be shared in order to promote openness and a healthy scientific culture.Indeed, scientists who are philosophically aligned with open science currently employ a range of data sharing practices (Fig. 2).A full embrace of open science implies sharing data instantaneously, or upon completion of initial quality assurance checks or other pre-processing (e.g., NEON; LTER, Taylor and Loescher 2013).In other cases, researchers have made an argument for a constrained period of exclusive access by researchers directly involved in data collection (e.g., Sloan Digital Sky Survey; http://www.sdss.org/).Despite these differences, it is increasingly recognized in the requirements of funding agencies that full data sharing in established repositories should begin no later than the publication of results.
Ecologists also have not yet converged on norms regarding ethical complications of sharing data that may cause harm.Ethical concerns are commonly cited as a rationale for not publishing locations or other information that may endanger sensitive species (Eschenfelder and Johnson 2014).Likewise, ecologists may be reluctant to share data that could harm people (e.g., by lowering property values).These issues are increasingly coming into focus as society grapples with the privacy concerns of satellites and drones capturing data at previously unimagined scales (Paneque- Ga ´lvez et al. 2014), and should be handled with due care in the establishment of data-sharing policies.

Transparency throughout the data life-cycle
Scientists publish their methodology as a means to enable reproducibility by others, but have traditionally had to judge which details were important to transmit within the limitations imposed by print journals.The increasing prominence of online-only, open-access journals with no page limits (Wardle 2012), and more generally the availability of online supplementary methods sections, gives scientists scope to detail their methods more fully.A broader suite of online tools now creates opportunities to share the code, data, and detailed decision-making processes that constitute the scientific endeavor.Taking advantage of these opportunities to make tacit knowledge explicit to others is a crucial part of performing reproducible science (Collins 2001, Ellison 2010) and provides the substantial additional benefit of exposing untested assumptions and unidentified confounding effects.
Workflow tools (Table 1) now make it possible for scientists to make nearly every stage of the research process transparent, from sharing the detailed rationale for an approach to publishing the data and code that generated analyses and figures.Detailed sharing of methods and code improves clarity, and personal communications regarding methods crucially improves trust (Collins 2001).Social media can permit these communications to happen in the open with time stamps that can establish provenance of ideas (Darling et al. 2013).Openness throughout the data life-cycle also provides the scientist with the opportunity to receive feedback from the rest of the scientific community and the general public, reducing redundancy and accelerating scientific inquiry (Byrnes et al. 2014), particularly for those scientists who actively recruit such feedback.
Additionally, transparency encourages rev www.esajournals.orgsearchers to converge on standard structures for data and code archiving (Table 1).Such convergence is particularly important for interdisciplinary science, in which the fragmentation of resources and practices along disciplinary boundaries can substantially hinder research.
Common standards and a shared, searchable infrastructure help make data sets not merely open but also discoverable, improving their reach and impact and helping scientists identify potential new collaborators.
Having said all this, scientists need not fear that open science is only for the exhibitionists among us; we recognize that there are many points in the scientific process when deep, sometimes solitary reflection is invigorating and productive.

Acceptance of critique
Failure is recognized as a normal and necessary part of the scientific process, and yet academic science is structured to reward only being right in public (Merton 1957), creating tension in practicing open science.The more open our science, the greater the chance that our mistakes as well as our insights will be public.This prospect can be frightening to contemplate; one study of physicists found that those practicing secrecy prior to publication often did so to avoid the risk of looking foolish (Gaston 1971).We suggest that embracing this tension gives us the opportunity to be better and more

Peerage of Science
Peerage of Science offers pre-publication formal peer review (and review of the reviews), which can then be sent on to participating journals.

Axios Review
Axios Review offers pre-publication formal peer review and appraisal of a manuscript's fit with targeted journals; reviews can then be sent on to participating journals.Publication DOI for code Code can be given a DOI and cited in the literature.For example, a Github repository can be assigned a DOI via zenodo.org.DOI for data Data uploaded to any of the numerous available online repositories will be assigned a DOI and is then citable by other researchers using that dataset.

TOOLS AND BEST PRACTICES TO ENABLE SHIFTS IN MINDSET AND PRACTICE
An open science mindset affects the entire scientific process, carrying responsibilities and offering benefits at each stage along the way (Fig. 2).Throughout the process, social media are used to publicly discuss ideas, hypotheses, experimental designs, data collection, analytical approaches, and eventually publication (Darling et al. 2013, Gewin 2013).Products are published in open repositories that provide stable identifiers, version control and time stamps (Noble 2009, Wilson et al. 2014).Version control systems allow scientists to retain snapshots of previous analyses for future reference, collaborate easily and track contributions, record ideas, and safeguard against the loss of code and data (Ram 2013), thus preserving the long-term integrity of the project even as collaborations form and shift.Stable identifiers (e.g., DOIs) for every product allow proper attribution and linking.All of these steps are undertaken with an eye to making our work reproducible and open to others, but all offer the immediate benefit of making our work reproducible to ourselves.Many of the tools mentioned in Table 1 have proprietary analogs (e.g., as SAS is to R), and afford many similar advantages, but exclusive use of open-source, free software maximizes access by other researchers.All of these tools give us access to a research group far bigger than a single lab, helping experimental designs to be improved and stimulating discussion of worthwhile new directions, connections, and approaches.
Data.-If we are committed to data stewardship, planning an experiment entails not only thinking through the physical manipulations involved but also working out how to capture and share the data and metadata that will enable others to effectively re-use that information.The open-source DMPTool (Table 1) offers guidance to scientists creating data management plansnow often a prerequisite for funding-and helps scientists find institutional resources for implementation.At the same time, ready access to data sets collected by other scientists can help focus our questions, by identifying gaps and opportunities, and improve our ability to answer them (e.g., by allowing us to estimate and plan for experimental uncertainties).Once data have been collected, the open scientist prepares the data set for use by others and documents its provenance, then deposits it in a community-endorsed repository (e.g., Knowledge Network for Biocomplexity, Dryad) (Ru ¨egg et al. 2014).Many software tools facilitate the sharing and documentation of v www.esajournals.orgdata as well.Tools created by the ROpenSci initiative allow integration of this process within R-based workflows with packages such as EML (metadata creation) and rfigshare (data sharing on figshare.com).User-friendly tools such as Kepler or VisTrails help document provenance, and Morpho provides an easy way to create standardized, machine-readable metadata using the Ecological Metadata Language (EML).This process ensures that the data will remain usable, accessible, and citable for years to come.It further allows our work to be recognized and integrated more effectively into the larger body of knowledge and ensures that, when we return to a project after a period away, we can pick up where we left off.
Research process.-Ifwe are committed to transparency, we document and share as much information about the actual research process as is feasible.Electronic lab notebooks (e.g., IPython notebooks) help track and share the reasoning behind our experimental and analytical decisions, as well as the final protocol and any deviations, and can be linked to the resulting data files to keep research organized.Adhering to the discipline of consistently, carefully, and thoroughly documenting the research process is an exercise in critical thinking, a constant reminder to check our assumptions and clarify our thinking.
Data analysis.-Duringdata analysis, reproducible, script-based methods (e.g., in R or Python) can be used for every step from importing raw data to analysis and production of figures and final manuscripts (e.g., FitzJohn et al. 2014).Such tools are essentially self-documenting along the way.However, they may still produce many separate scripts, which would have to be executed in sequence.Workflow systems, like Kepler or VisTrails, can provide a more complete record of data manipulations.This type of record is almost impossible to generate for point-and-click analyses in a graphical user interface (GUI).While errors can be made in both scripted and GUI-based analyses, the existence of a record makes errors in the former far easier to detect and correct, protecting the integrity of the analysis (Leek and Peng 2015).Literate programming tools such as Sweave and knitr facilitate integration of data analysis into manuscript production, making it easier to keep figures and reported results current as an analysis is refined.
Publication.-Presentations,posters, figures, and movies can be opened for comment on public websites (e.g., Figshare, SlideShare).Publication preprints can be posted for comment from an audience broader than a journal's handful of peer reviewers; preprints also improve a project's visibility and, with the addition of a date stamp, establish precedence (Desjardins-Proulx et al. 2013)

CONCLUSIONS
Online tools make possible a future in which not only scientific practice but also scientific culture is transformed by openness (Nielsen 2011).Fully open science can take place throughout the process of discovery, from the sharing of nascent ideas, to the uploading of data at the moment of capture, through to developing ''living papers'' in an open forum in which the details of analysis and reasoning are completely transparent.Subsequent generations of ecologists will build their work on what we leave.If, instead of exclusive silos of traditional journal archives, we leave future researchers open-access repositories of data, code, and papers, they will be far better equipped to push new frontiers in science and create solutions to pressing societal problems.
Very real technological and cultural hurdles still stand between us and this future: investigators must be willing to invest time in learning the tools that facilitate open science, and in relearning them as the tools evolve.Further, the scientific community must collectively establish new norms for collegiality and reproducibility in the digital age.Nevertheless, we can all move our research toward this future by adopting the aspects of open science that are currently feasible for our own research groups (e.g., publishing open-access articles; sharing all data and code used in publications) and by supporting our students and junior colleagues in developing the skills that will best prepare them for the v www.esajournals.orgresponsibilities, opportunities, and rewards of practicing ecology in an open environment.
''A journey of a thousand miles begins with a single step'' -Lao-tzu, Tao Te Ching employing standards-based technology tools.Frequently encompasses all of open access, open data and open source and, minimally, facilitates reproducibility of results.

Fig. 1 .
Fig. 1.Increasing usage of the term ''open science'' in the literature since 1995 in Web of Science and PubMed databases.Data from PubMed were downloaded via the rentrez (Winter and Chamberlain 2014) package in R, and Web of Science data were collected from manual searches.Results were normalized by total articles published each year to account for the increasing number of publications.Both data sources show an increase in the number of publications about open science, and an increase in annual citations of those papers.

Fig. 2 .
Fig. 2. Three examples of possible open science workflows.In each workflow illustration, the gray box surrounds activities that are not openly accessible for researchers who are not directly involved.Activities outside these boxes are open and available, representing how the individual researcher is influenced by other scholars, or is able to communicate their research before and after publication.White boxes represent distinct research products available for reference for and feedback from other researchers.For a historical antecedent of this diagram, from the field of psychology, seeGarvey and Griffith (1964).

Table 1 .
A wide range of tools is available to support open science at each stage of the research life-cycle.Tools change over time and these are some but not all of those available at the time of this publication.Note that several of these tools, like Twitter, may fit under more than one concept.While tools change over time, the concepts underlying shifts toward open science are likely to remain.

Table 1 .
Continued.Cold Spring Harbor, is a relatively new preprint server that focuses primarily on biological research.arXiv arXiv is one of the original preprint servers on the web.Run by Cornell, it is mainly focused on math, physics, and computer science, although it has been used by quantitative biologists as well.
. Publishing final papers in open-access journals (''gold'' open access) or self-archiving manuscripts (''green'' open access) makes the final products available to a wide audience, including the taxpayers who may have funded the research.