OpinionArchiving Primary Data:Solutions for Long-TermStudiesJames A. Mills,1,#,* Céline Teplitsky,2,#,* Beatriz Arroyo,3

Anne Charmantier,4 Peter. H. Becker,5 Tim R. Birkhead,6

Pierre Bize,7 Daniel T. Blumstein,8 Christophe Bonenfant,9

Stan Boutin,10 Andrey Bushuev,11 Emmanuelle Cam,12

Andrew Cockburn,13 Steeve D. Côté,14 John C. Coulson,15

Francis Daunt,16 Niels J. Dingemanse,17,18 Blandine Doligez,9

Hugh Drummond,19 Richard H.M. Espie,20

Marco Festa-Bianchet,21 Francesca Frentiu,22

John W. Fitzpatrick,23 Robert W. Furness,24 Dany Garant,21

Gilles Gauthier,14 Peter R. Grant,25 Michael Griesser,26

Lars Gustafsson,27 Bengt Hansson,28 Michael P. Harris,16

Frédéric Jiguet,29 Petter Kjellander,30 Erkki Korpimäki,31

Charles J. Krebs,32 Luc Lens,33 John D.C. Linnell,34

Matthew Low,35 Andrew McAdam,36 Antoni Margalida,37

Juha Merilä,38 Anders P. Møller,39 Shinichi Nakagawa,40

Jan-Åke Nilsson,27 Ian C.T. Nisbet,41 Arie J. van Noordwijk,42

Daniel Oro,43 Tomas Pärt,35 Fanie Pelletier,21 Jaime Potti,44

Benoit Pujol,13 Denis Réale,45 Robert F. Rockwell,46

Yan Ropert-Coudert,47 Alexandre Roulin,48

James S. Sedinger,49 Jon E. Swenson,50

Christophe Thébaud,12 Marcel E. Visser,42 Sarah Wanless,16

David F. Westneat,51 Alastair J. Wilson,52 andAndreas Zedrosser53

The recent trend for journals to require open access to primary data included inpublications has been embraced by many biologists, but has caused apprehen-sion amongst researchers engaged in long-term ecological and evolutionarystudies. A worldwide survey of 73 principal investigators (Pls) with long-termstudies revealed positive attitudes towards sharing data with the agreement orinvolvement of the PI, and 93% of PIs have historically shared data. Only 8% werein favor of uncontrolled, open access to primary data while 63% expressed seriousconcern. We present here their viewpoint on an issue that can have non-trivialscientific consequences. We discuss potential costs of public data archiving andprovide possible solutions to meet the needs of journals and researchers.

Trends in Ecology & Evolution, October 2015, Vol. 30, No. 10 http://dx.doi.org/10.1016/j.tree.2015.07.006 581© 2015 Elsevier Ltd. All rights reserved.

TrendsPublic data archiving is the archiving ofprimary data used in publications sothat they can be preserved and madeaccessible to all online.

Public data archiving is increasinglyrequired by journals. However, thecosts of public data archiving mightbe underestimated, in particular withrespect to long-term studies.

Long-term studies have been respon-sible for the answers to many importantquestions in evolution and ecologywhich could only be answered throughfollowing the life-histories of individualsfor decades.

Several papers have been published infavor of public data archiving, but amore balanced viewpoint is necessaryto allow a discussion to emerge on acode of ethics and ways to preserveand protect the data, encourage theinitiation and continuation of long-termstudies, and meet the requirements ofthe whole scientific community.

110527A Skyline Drive, Corning, NY14830, USA2Département Ecologie et Gestion dela Biodiversité, UMR 7204 CNRS/MNHN/UPMC, Muséum Nationald’Histoire Naturelle, Paris, France3Instituto de Investigacion enRecursos Cinegeticos (IREC) (CSIC-UCLM-JCCM), Ronda de Toledo s/n,13005 Ciudad, Real, Spain4Centre d’Ecologie Fonctionnelle etEvolutive UMR 5175, Campus CNRS,1919 Route de Mende, 34293Montpellier CEDEX 5, France5Institute of Avian Research,‘Vogelwarte Helgoland’, An derVogelwarte 21 D26386 Wilhelmshaven,Germany6Department of Animal and Plant

Long-Term Data SharingSeveral funding agencies, international regulatory bodies, and many major ecological andevolutionary journals now require raw or primary data to be deposited in a permanent openaccess archive, such as Dryad or TreeBASE, as a condition for funding or publication. The datamust be in sufficient detail to allow the analyses in the paper to be replicated. The rationale foropen archiving is that archived data are available to posterity when studies are completed, forerror-checking, for use in new studies, or for future meta-analysis [1]. In addition it has beenargued that the policy would benefit data providers by increasing their citation index throughcitations by papers with new analyses [1,2].

Although it is claimed that over 95% of scientists in evolution and ecology believe that datashould be publicly archived [1], mandatory public data archiving (PDA) is raising many issuesin the scientific community as evidenced by debates on websites, in blogs, and in publications([2–9]; McGlynn, T. (2014) I own my data, until I don’t. http://smallpondscience.com/2014/03/03/i-own-my-data-until-i-dont/). We focus on the perspective from long-term individual-basedstudies of wild populations that often span several decades.

Short and long-term ecological studies differ in several important aspects. For example, in theformer, data tend to be collected over a short period of time leading to one or two publications,and once published the data in these papers become less valuable to the collector and can bemore useful to others with different perspectives or analytical skills. By contrast, in studies thathave followed individuals over their lifetimes, a great deal of crucial information is assessed fromderived metrics (e.g., survival, lifetime reproductive success) that can only be estimated aftermany years of fieldwork. Therefore, much value can remain in the primary data even after someof the initial questions have been answered.

Long-term studies are rare and have great scientific value because many important questions inecology and evolutionary biology can only be answered from the life-histories of recognizableindividuals [10]. A detailed analysis of the importance of individual-based studies has beendocumented elsewhere [10], but a few examples are given in Box 1.

While group discussions and blog posts on PDA-related issues have been flourishing, little isformally known and published about the position and concerns of people collecting long-termdata. To fill this gap, a survey was conducted to learn their perspectives, and if current datarequirements were perceived as being problematic, to identify potential alternative data-sharingpolicies that could be acceptable to the journals, the scientific community, and the PIs.

The SurveyTo obtain the opinions of scientists with individual-based longitudinal data, a worldwide surveywas sent to 146 PIs of long-term research projects. Responses were received from 73 PIs

Sciences, University of Sheffield,Sheffield, UK7Institute of Biological andEnvironmental Sciences, University ofAberdeen, Aberdeen, UK8Department of Ecology andEvolutionary Biology, University ofCalifornia, 621 Young Drive South,Los Angeles, CA 90095-1606, USA9CNRS,Université Lyon 1, Universitéde Lyon, UMR 5558, LaboratoireBiométrie et Biologie Évolutive, 43boulevard du 11 Novembre 1918,69622 Villeurbanne CEDEX, France10Department of Biological Sciences,University of Alberta, Edmonton,

Box 1. Ecological and Evolutionary Importance of Long-Term Studies

Studies that have followed individuals throughout their lives have yielded important insights into demographic and life-history parameters of wild populations which cannot be obtained from cross-sectional programs. They have provideddetails on the impact of age, individual quality, status of pair-bond and food abundance on aspects of breeding,recruitment and survival [11–24]; cost of breeding [25]; inbreeding [26–28]; senescence [29–30]; mate choice [31–32];carry-over and transgenerational effects [33–37] and lifetime reproduction [38–39]. Studies that assembled pedigreesfrom observational and or molecular techniques have enabled widespread application of quantitative genetic methods toquestions in evolutionary ecology, such as maintenance of genetic variance, inheritance of fitness components and therelative contribution of plasticity and micro-evolutionary processes to phenotypic change [40–47]. Importantly, long-termstudies have also been the basis for understanding the impact of climate change [48–51], habitat loss and naturalresource overexploitation [52]. To address many of the aspects or issues listed above, researchers must have access to amarked age-structured and pedigreed study population which can take a minimum of 10 to 20 years of monitoring toestablish, depending on the generation time of the species.

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Alberta T6G 2E9, Canada11Department of Vertebrate Zoology,Faculty of Biology, LomonosovMoscow State University, LeninskieGory 1/12, 119234 Moscow, Russia12UMR 5174 EDB LaboratoireÉvolution et Diversité Biologique,CNRS, ENFA, Université Toulouse 3Paul Sabatier, 31062 Toulouse CEDEX9, France13Department of Evolution, Ecologyand Genetics, Research School ofBiology, The Australian NationalUniversity, Canberra, ACT, Australia14Département de Biologie and Centred’Etudes Nordiques, Université Laval,1045 avenue de la Médecine, QuébecG1V 0A6, Canada1529 St Mary's Close, Shincliffe,Durham DH1 2ND, UK16Centre for Ecology and Hydrology,Bush Estate, Penicuik, EH26 0QB UK17Behavioural Ecology, Department ofBiology, Ludwig-MaximiliansUniversity of Munich, Planegg-Martinsried, Germany18Evolutionary Ecology of VariationResearch Group, Max Planck Institutefor Ornithology, Seewiesen, Germany19Departamento de Ecología Evolutiva,Instituto de Ecología, UniversidadNacional Autónoma de México, AP70-275, México DF 04510, México20Technical Resource Branch,Saskatchewan Ministry ofEnvironment, 3211 Albert Street,Regina, Saskatchewan, S4S 5W6,Canada21Département de Biologie, Universitéde Sherbrooke, 2500 Boulevard del’Université, Sherbrooke, Québec J1K2R1, Canada22School of Biomedical Sciences andInstitute of Health and BiomedicalInnovation, Queensland University ofTechnology, Kelvin Grove, QLD 4059Australia23Cornell Lab of Ornithology, 159Sapsucker Woods Road, Ithaca, NY14850, USA24Graham Kerr Building, University ofGlasgow, Glasgow G12 8QQ, UK25Department of Ecology andEvolutionary Biology, PrincetonUniversity, Princeton, NJ 08544-1003,USA26Anthropological Institute andMuseum, University of Zürich, Zürich,Switzerland27Department of Animal Ecology,Evolutionary Biology Center, UppsalaUniversity, Uppsala, Sweden28Department of Biology, LundUniversity, Ecology Building, 223 62,Lund, Sweden29CESCO, UMR7204 SorbonneUniversités-MNHN-CNRS-UPMC,CP51, 55 Rue Buffon, 75005 Paris,France

1–4 10 –14 20 –24 30 –34 40 –44 50 –54 60 –640

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Figure 1. Duration of Studies Undertakenby the Respondents in this Survey.

working on 59 bird studies, 13 mammalian studies, and 1 plant study. The 92 projects (some PIshave several projects) range in duration from 5 to 68 years (Figure 1), with 55% collecting data formore than 30 years. Thirty-five percent of researchers were required to archive data used in apublication by their current funding agency and 19% by their institution. Eight researchers wererequired to deposit data by both; therefore 59% were not required to archive their data. Therewas diversity of opinion among PIs about data archiving, but some strong points of consensusemerged. This paper synthesizes the views of all respondents, many of whom have madeimportant contributions to ecology and evolution.

The survey revealed that virtually all PIs were in favor of data sharing with the agreement orinvolvement of the PI. Historically, 93% of the respondents have shared their data when askedand 80% have collaborated in meta-analyses. In the 1960s to 1970s publications usinglongitudinal data often involved only one or two authors. However, over the past two decadesstudies have become more complex and collaborative, with studies commonly involving col-laboration among biologists with expertise in a variety of disciplines.

Overall, 63% of PIs were against PDA as currently required. This contrasts with a previous surveyof ecological and evolutionary biologists that reported that 95% were in favor of PDA [1]. Amongthe 36% of respondents in favor of open-access data-archiving in this survey, only six (8% of 73)were in favor of unconditional data archiving. The reasons given by PIs in favor of PDA weresimilar to those advocated by the archiving journals. By contrast, 91% of PIs supported datasharing when clear rules for data access were in place. These rules could include (i) coauthorshipor at least acknowledgment, depending on the level of PI involvement; (ii) no overlap with currentprojects, particularly projects conducted by students or postdoctoral fellows; and (iii) anagreement that the data go no further than the person to whom they are entrusted.

General Concerns about PDAThe main issues about archiving were centered on what data would be archived and to whomaccess would be given, as detailed below. However, these concerns are so strong that 41% ofrespondents said that they have avoided publishing in journals that require data be deposited inopen-access archives. Furthermore, 53% intend to avoid publishing in them in the future and, forthose who published a major paper involving long-term data early in their careers, 63% indicatedthat they would not have submitted it to any journal that required data archiving. Avoidingpublishing in a high-impact journal can have major consequences in terms of career advance-ment, and could potentially reduce the prospects of obtaining future financial support; thereforethe decision would not be taken lightly.

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30Grimso Wildlife Research Station,Department of Ecology, SwedishUniversity of Agricultural Sciences(SLU) 73091, Riddarhyttan, Sweden31Section of Ecology, Department ofBiology, University of Turku, 20014Turku, Finland32Department of Zoology, University ofBritish Columbia, Vancouver, BritishColumbia V6T 1Z4, Canada33Terrestrial Ecology Unit, Departmentof Biology, Ghent University,Ledeganckstraat 35, 9000 Gent,Belgium34Norwegian Institute for NatureResearch, PO Box 5685 Sluppen,7485 Trondheim, Norway35Department of Ecology, SwedishUniversity of Agricultural Sciences,75007 Uppsala, Sweden36Department of Integrative Biology,University of Guelph, Guelph, Ontario,N1G 2W1, Canada37Faculty of Life Sciences andEngineering, University of Lleida,25198 Lleida, Spain38Ecological Genetics Research Unit,Department of Biosciences, PO Box65 (Biocenter 3, Viikinkaari 1),University of Helsinki, 00014 Helskinki,Finland39Laboratoire Ecologie, Systématiqueet Evolution, Equipe Diversité,Ecologie et Evolution Microbiennes,Bâtiment 362, 91405 Orsay CEDEX,France40Evolution and Ecology ResearchCentre and School of Biological, Earthand Environmental Sciences,University of New South Wales,Sydney, Australia41I.C.T. Nisbet and Company, 150Alder Lane, North Falmouth, MA02556, USA42Department of Animal Ecology,Netherlands Institute of Ecology(NIOO-KNAW), PO Box 50, 6700 ABWageningen, The Netherlands43Institut Mediterrani d’EstudisAvançats IMEDEA (CSIC-UIB), MiquelMarques 21, 07190 Esporles,Mallorca, Spain44Departamento de Ecologia Evolutiva,Estación Biológica de Doñana-CSIC,Av. Américo Vespucio s/n, 41092Seville, Spain45Département des SciencesBiologiques, Université du Québec AMontréal, CP 8888 Cuccursale CentreVille, Montréal, Québec H3C 3P8,Canada46Vertebrate Zoology, AmericanMuseum of Natural History, New York,NY 10024 USA47Institut Pluridisciplinaire HubertCurien, CNRS UMR7178, 23 rueBecquerel 67087 Strasbourg, France48Department of Ecology andEvolution, University of Lausanne,

In discussions among the survey respondents, it was suggested that the design and datacollection of a long-term study constitute a research infrastructure that is the foundation ofthe publications which form the lifework and careers of researchers, PhD students, andpostdoctoral fellows who work on these programs. The analogy can be made to experimen-tal infrastructures which involve the construction of an apparatus that takes years, orsometimes decades, and requires numerous grant applications, institutional support, anddeferred publication effort, all of which involve significant risk, but potentially have profoundscientific value, both pure and applied. Developing the infrastructure is a necessary prereq-uisite for project completion. In this case it would not be reasonable for other scientists tohave immediate access to the fruits of the inventor's labors. Furthermore, compulsory andunrestricted open access to the apparatus would provide a strong disincentive to making theinitial infrastructural investment. The same case can be made for long-term ecologicalstudies.

Specific Concerns from Long-Term Researchers about PDASeveral concerns about the costs of PDA for researchers and the scientific community wereaddressed previously [5]. We add here the perspective of PIs with long-term studies. Threemajor concerns were identified during the survey.

Potential Costs to ScienceFlawed Science. A major cost would be flawed science resulting from a lack of understandingof the database or the biological system. Open access to long-term data might not allowfull understanding of all the subtle contexts, nuances, and issues involved in the biologicalsystem and the structure of the database from which the long-term data are collected. It hasbeen argued that if method sections are sufficiently detailed, misunderstanding the systemshould not be a major source of error [Coulson, T. and Sheldon, B. (2014) Archive your data!Animal ecology in focus. https://journalofanimalecology.wordpress.com/2014/11/21/archive-your-data/]. However, not all of the complexities of the biological system can bedetailed in a method section without making a paper unwieldy. Hence, without the involve-ment of the PI, crucial contextual information is likely to be lost under open access, leading tothe potential for erroneous assumptions and interpretations which could add to the growingretraction rate in scientific journals [53]. For example, although it was not included as aquestion, three respondents of the survey indicated that on four occasions their data havebeen misinterpreted in publications and, once published, errors or misinterpretations arehard to remove.

More Time Spent on Redundant ActivitiesA potential cost would be simultaneous testing of the same idea on the data. In some cases,hypotheses might have been already investigated but not published by the Pls because theywere inconclusive. In addition, the cost of monitoring publications that used PDA and writingreplies would be borne by the researcher with long-term data and not by the scientificcommunity. These do not seem to be a productive use of research investment.

Fewer Long-Term StudiesOpen-access archiving could reduce the incentives for carrying out long-term studies and wouldlikely result in researchers suspending ongoing studies and declining to undertake new ones.This is predicted by the producer–scrounger game theory [54] where the producer spends timeand energy to develop a resource but is unable to monopolize it, thereby creating opportunitiesfor the resource to be exploited by scrounger(s). Over time, as the scrounger strategy increases,the resource decreases. In theory, the fitness of the producer and the scrounger decreasebecause at some point there are no more resources to scrounge because no more resourcesare being produced [55,56].

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Lausanne, Switzerland49Department of Natural Resourcesand Environmental Science, Universityof Nevada Reno, Reno NV 89512,USA50Department of Ecology and NaturalResource Management, NorwegianUniversity of Life Sciences, PO Box5003, 1432 Ås, and Norway andNorwegian Institute for NatureResearch, PO Box 5685 Sluppen,7485 Trondheim, Norway51Department of Biology, Center forEcology, Evolution, and Behavior,University of Kentucky, Lexington, KY,USA52Centre for Ecology andConservation, College of Life andEnvironmental Sciences, University ofExeter, Cornwall Campus, PenrynTR10 9EZ, UK53Faculty of Arts and Sciences,Department of Environmental andHealth Studies, Telemark UniversityCollege, 3800 Bø i Telemark, Norway

Less CollaborationNew collaborations are extremely valuable to make the most of the data, but comparativeanalyses and meta-analysis among long-term studies would likely suffer because PIs mightdecline to participate if they are required to archive their data.

Research FundingSeveral financial issues have been overlooked by the advocates of PDA. Archiving mutualizes thebenefits, but not the costs of long-term studies, because there is no cost to the personaccessing the data. This might be a sustainable model when recurrent funding is available,but not when funding is granted on a per project basis. In addition, PDA could incur some newcosts for long-term studies because Dryad, for example, has required extra payment for largedatasets. Researchers with scarce funding might not be able to absorb this additional cost.Maintaining constant funding is a crucial issue for long-term studies to avoid fatal gaps in the data[10,57], contrasting once again with short-term studies that can be restarted at a later time.Long-term studies of all durations experienced difficulties with funding (Figure 2) because only33% were fully funded in all years, with the remainder having funding gaps varying in durationfrom 1 to 19 years (Figure 2). To maintain funding, PIs with long-term projects must keepidentifying new uses of the data to obtain short-term funding because recurrent funding isessentially nonexistent [10]. Therefore, PDA could lead to a loss of funding opportunities if datafor their next project are routinely mined by other researchers.

Student Experience and TrainingA major contribution of long-term studies is that they often provide training to PhD and otherpostgraduate students and postdoctoral fellows. The PIs that responded to the survey reportedthat, from their 92 projects, 630 PhDs were awarded (Figure 3A), and 658 postgraduates and257 postdoctoral fellows participated, for a total of 1545 trainees. This represents a substantialcontribution to the training and development of the ecological and evolutionary biology researchcommunity. Survey respondents expressed a particular concern that PDA would negativelyimpact upon this important feature of long-term studies because negotiations take place amongstudy participants before the onset of new research areas (such as MSc and PhD thesis orpostdoctoral research projects) to avoid overlap. Such planning is undermined if outsiders areentirely free to work with available data from long-term studies without taking ongoing andplanned analyses by insiders into account. The risk is especially strong for PhD studentsbecause part of their training involves courses, and they need more time to complete theresearch project and publish papers than do senior researchers.

*Correspondence: dmills@stny.rr.com(J.A. Mills), teplitsky@mnhn.fr(C. Teplitsky).#J.A.M. and C.T. contributed equally.

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Figure 2. Duration of the Study and thePercentage of Years Unfunded.

Trends in Ecology & Evolution, October 2015, Vol. 30, No. 10 585

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Figure 3. (A) The Total Number of PhDStudents in Relation to the Duration ofResearch Programs. (B) The Number ofPapers Produced in Relation the Durationof the Study.

Possible SolutionsThe verification of results is a very important requirement by journals; however, the costs ofmandatory archiving of data by ongoing long-term projects could outweigh the expectedbenefits. Having imposed a requirement for PDA, journals are asking researchers to give uprights to what many consider to be their intellectual property. In fact, some scientists areconsidering copywriting their data. Journals are rightly vigilant in combating plagiarism andcopyright infringement; it would be appropriate for journals to be equally vigilant in respectingand protecting the scientists’ data.

A resolution to this conflict would benefit scientific progress; high-quality long-term studies havebeen responsible for a disproportionate number of publications in journals with the highestimpact factors [10]. Many of the 5378 papers from 90 studies in this survey (Figure 3B) werepublished in prestigious journals that now require PDA. To initiate a discussion about howresolution might be achieved, we suggest six potential solutions.

Promoting CollaborationOpportunities for collaboration that provide added-value to science and communicationbetween data generators and potential users should be encouraged [5] rather than compulsoryarchiving. Most survey respondents see collaborations as the most satisfactory route to data

586 Trends in Ecology & Evolution, October 2015, Vol. 30, No. 10

sharing. For substantial requests, the original researcher can expect and deserve coauthorship.To promote better use of data and collaboration with Pls, a website could be created referencinglong-term studies with information such as species, duration of study, location, traits measured,and protocols used.

Providing Primary Data on a Confidential BasisA solution that would satisfy most PIs would be to provide tabulated summary data initially, and ifthose data were insufficient for editors to evaluate a submitted paper, primary data could beprovided on a confidential basis. After the review process, the data could be destroyed andwould not be available to be used for any other purpose. Once the paper is published, peoplewho want to use the data could contact the Pls of the long-term study for additional data. As thesurvey has shown, 93% of the respondents have indicated that they have supplied data onrequest. For example, researchers have used summary data from the 40 year study on Darwin'sfinches [44,58] by Peter and Rosemary Grant which was deposited in Dryad, and raw data havebeen supplied to four others upon request.

Providing a Longer EmbargoSome journals have indicated a willingness to embargo the data for a period of 1–5 years frompublication, allowing the original researcher time to complete any related papers. This canreduce concerns in the case of smaller datasets from which only a limited number of questionscan be answered. However, this is unlikely to solve the problem for long-term datasets, fromwhich many questions can be addressed from different perspectives and over differing lengthsof time.

For active long-term studies (i.e., with ongoing data collection) a minimum of 10–15 yearsmight be considered more appropriate [5]. By comparison, pharmaceutical companies havea 20 year patent to recoup their investment. A similar argument could be made for the decadesof research by long-term project scientists [McGlynn, T. (2014) I own my data, until I don’t.http://smallpondscience.com/2014/03/03/i-own-my-data-until-i-dont/]. Furthermore, a longerembargo would encourage data users to contact the PIs for rapid access to the most up-to-dateversion of the database, thereby encouraging collaboration. For non-active studies wheredata collection has ended, the case for an earlier release is stronger.

Depositing Data on Institutional ServersCentralizing the data in a single database in one location will prevent fragmentation of data ondifferent archiving sites and ensure that the data are completely secure and up to date. Datacould be archived on institutional servers, and the institution and its staff could control accessand determine if collaboration is appropriate. An example of an effective approach to themanagement of archived data held by institutions is practiced by The Netherlands Instituteof Ecology where people can request the data, and data extraction is carried out by membersof the Institute, provided that the applicant will use the data for a well-described project, committo not sharing the data with others, and offer coauthorship to the collector if the data forms anessential part of the publication. Another example of effective use of institutional servers is theArchibold Biological Station in Florida. Such institutional databases also allow the preservationof data and their accessibility after the Pl retires [10].

Increasing Notification and CommunicationIf online archiving should be preferred for the physical safety of data, two improvements topresent practices could be made. First, as the survey demonstrated, PIs are concerned withinappropriate use of data and overlap with ongoing or future projects of their own. A clear policyshould be implemented by journals concerning conflicts of interest between the researcherscollecting and organizing the data, and those who would use the data. For example, there are

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Outstanding QuestionsHow long can long-term studies con-tinue to flourish with a requirement topublicly archive data? Providing publicaccess to the data disadvantagesthose who invest time and resourcesin the collection and maintenance oflong-term data.

Will journals and scientists with long-term studies be able to develop andimplement an approach to data archiv-ing that is acceptable to both? Collab-oration, longer embargo and a code ofethics on data usage are componentsof a potential solution.

What are the implications of copyright-ing long-term datasets? Copyrightingtheir datasets would allow scientists toprotect their intellectual property in thesame way that journals protect theirpublications.

currently no binding protocols or codes of conduct covering the presentation of, or access to,complex data that underpin analyses in publications. A process with guidelines should beestablished by journals to ensure that PIs are aware of potential studies and are satisfied with apaper based on the data they generated before the review process.

A possibility would be to implement data-tracking, allowing data collectors to obtain informationon who is using the data and why. For example, any request for data to the Climate Change,Agriculture, and Food Security Data Portal triggers an email to be sent to the PI who depositedthe data. Journals should have a rule that no paper is considered where the data users have notcorresponded with the data owners and included appropriate acknowledgement of the sourceof the data within the paper. A rule set by journals would have a great deal of clout with datausers. Data tracking would also allow the PI to be systematically asked to review papers basedon their data. Another option would be to send an email to the PI every year asking whether theywish the data to be private or open access.

Concluding RemarksLong-term studies currently generate science with high impact in all major fields of biology.These longitudinal studies began during an era when PDA did not exist. Although we agree that itis essential to archive data so that they are not lost to science, a key concern is that recentlyintroduced data-archiving regimes combined with difficulty in obtaining continuous financialsupport will be a disincentive both for the initiation of long-term studies, and for maintenance ofongoing studies. It would be appropriate for journals and data-archiving institutions to enter intoa dialog with researchers about how best to meet the objectives of data archiving while allowingvaluable long-term studies to thrive.

Specifically, we recommend the development of a formal code of conduct which respects thedata generated through long-term studies, and (i) allow tabulated summaries to be provided inthe first instance backed up by the confidential submission of primary data if required by editors,(ii) encourage collaborative research with the data collector by people wishing to use the data, (iii)extend embargoes on the use of archived data [5], (iv) consider allowing archiving on institutionalservers rather than open-access servers, and (iv) develop enforceable procedures that enablethe researcher to be contacted when someone wishes to access primary data. Through thesemodifications, a compromise could be crafted that provides an advantage to the scientificcommunity, journals, and researchers generating long-term data, as well as benefiting science.

AcknowledgmentsWe wish to thank all of the principal investigators who provided information on their long-term studies. C.T. was funded by

the French Agence Nationale de la Recherche (grant ANR-12-ADAP-0006). Many thanks to Sandra Hamel, Susan Alberts,

and Walt Koenig for constructive comments. Deborah Mills assisted in the analysis and editing the manuscript.

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LetterA Balanced DataArchiving Policy forLong-Term StudiesMichael C. Whitlock,1,*Judith L. Bronstein,2

Emilio M. Bruna,3,4

Aaron M. Ellison,5

Charles W. Fox,6

Mark A. McPeek,7

Allen J. Moore,8

Mohamed A.F. Noor,9

Mark D. Rausher,9

Loren H. Rieseberg,10

Michael G. Ritchie,11 andRuth G. Shaw12

Long-term monitoring and experimentsare crucial to understanding many impor-tant questions in ecology and evolution,and, consequently, the data sets thatemerge from long-term projects can beextremely valuable. It is crucial that suchdata are treated in a way that supports thebest interests of science. We must con-tinue to encourage researchers to engagein long-term projects, and we must alsoensure that such data are widely availablein perpetuity [1,2]. Balancing these some-times opposing goals is a difficult but notinsurmountable problem, and certainlyone that should be resolved in a way thatbalances the needs of those who pro-duced those data with the best interestsof science.

In a recent article in TREE, Mills et al. [3]argued that current data accessibility poli-cies hinder long-term studies. They raisedseveral important issues. While many of usstrongly disagree with many of the pointsthat they raised, we do think that somechanges to data-archiving policies arewarranted.

The current data-archiving policies ofmany ecology and evolution journals have

provisions to attenuate the burdens ofdata archiving. First, the current policiesdo not require archiving of the entire dataset from a project; they require only thatauthors make available the data neces-sary to recreate the analyses and resultsin the published manuscript. Second,embargoes of public access to archiveddata for a year after publication are typi-cally automatic, but longer embargoescan be allowed with the discretion of theeditor. However, while we think that edi-torial discretion is an important tool in a fairpolicy, such discussions can be inefficientand lead to inconsistent policies.

Despite these existing provisions, we doagree with Mills et al. that, in some situa-tions, the current data-archiving policyadopted by many ecology and evolution-ary biology journals does not adequatelybalance the needs of scientists producinglong-term data sets with the needs of thecommunity. As some of the originalframers of the joint data archiving policy[1] and current editors of ecology andevolution journals, we propose the follow-ing as a balanced way forward (in manycases echoing the suggestions of Rocheet al. [4]):

� As Mills et al. [3] suggest, a longerembargo period may often be appropri-ate for long-term studies. We suggestthat, for projects for which the key datareported in the publication have beenregularly collected from a population formore than 5 years, journals should allowa 5-year embargo period upon authorrequest. This longer embargo allowsauthors the opportunity to make addi-tional use of their own data while ensur-ing that the data underlying results in thepaper are appropriately preserved andeventually available for reuse.

� With longer embargoes, the importanceof careful data management and goodmeta-data becomes even greater,because the data cannot be easily vet-ted while the potential ambiguities arefresh in the authors’ minds. Authors

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who opt for a longer embargo shouldtake care that the data being archivedare well presented for easy and unam-biguous reuse in the future.

� As Mills et al. also note [3], original datacollectors have insights into the datathat cannot be fully extracted from pre-vious papers and metadata. Journalsand researchers who reuse data shouldrecognize that, in most cases, data willbe better understood and analyzed withthe cooperation or collaboration ofthose who collected the data. We agreethat reusers of data should stronglyconsider consulting and, in manycases, directly collaborating [1_TD$DIFF] with [16_TD$DIFF],depositors on new data analyses. How-ever, we do not feel that this should be amandatory policy, and such consulta-tion will be less needed when the dataare reused as a part of a larger meta-analysis ( [17_TD$DIFF]see [5]).

� For substantial reanalyses of data setsthat do not include original data collec-tors as authors, journals shouldendeavor to enlist one or more of theoriginal data collectors as reviewers, asMills et al. suggest [3]. Obviously, thispractice has the potential for abuse.However, reviews from data collectorswill, in most cases, be invaluable forassessing the appropriateness of thedata set for the questions beingaddressed in the new analysis.

� Scientific funders should make clearthat long-term projects are valued,especially when the data from themare broadly available for reuse within areasonable time frame. All scientificproducts made possible by the datasets, whether produced by the originaldata collectors or others, should becounted when assessing the returnon investment of grants supportinglong-term projects. We also think thatit is reasonable and responsible for fun-ders to set stricter standards on theopenness of data than we suggestabove [18_TD$DIFF] for journals.

Data archiving allows the scientificcommunity to produce new results

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TREE 2032 No. of Pages 2

economically [6] and permits the essentialverification of existing results [7]. Withoutpublic archiving, data are lost [8] or simplynot shared [9]. If journals provide moreclarity, unity, and flexibility for longerembargoes for long-term data sets, theincentive to collect long-term data canbe retained while still ensuring that thevaluable data from long-term studies willnot be lost to the broader scientificcommunity.

1Department of Zoology, University of British Columbia,

Vancouver,[2_TD$DIFF] V6T 1Z4, Canada2Department of Ecology and Evolutionary Biology,

University of Arizona, Tucson, AZ [5_TD$DIFF]85721, USA3Department of Wildlife Ecology and Conservation,

University of Florida, PO Box 110430, Gainesville, FL

32611-[6_TD$DIFF]0430, USA

2 Trends in Ecology & Evolution, Month Year, Vol. xx, No. y

4Center for Latin American Studies, University of Florida,

PO Box 11530, Gainesville, FL 32611-5530, USA5Harvard Forest, Harvard University, Petersham, MA

01366, USA6Department of Entomology, University of Kentucky,

Lexington, KY 40546-0091, USA7Department of Biological Sciences, Dartmouth College,

Hanover, NH, USA8Department of Genetics, University of Georgia, Athens,

GA[7_TD$DIFF] 30602, USA9Department of Biology, Duke University, Durham, NC[7_TD$DIFF]

27708, USA10Department of Botany, University of British Columbia,

Vancouver,[2_TD$DIFF] V6T 1Z4, Canada11School of Biology, University of St Andrews, St

Andrews[10_TD$DIFF], KY16 9AJ, UK12Department of Ecology, Evolution and Behavior,

University of Minnesota, Minneapolis, MN [13_TD$DIFF]55108, [14_TD$DIFF]USA

*Correspondence: whitlock@zoology.ubc.ca

(M.C. Whitlock).

http://dx.doi.org/10.1016/j.tree.2015.12.001

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References1. Whitlock, M.C. et al. (2010) Data archiving. Am. Nat. 175,

145–146

2. Bruna, E.M. (2010) Scientific journals can advance tropicalbiology and conservation by requiring data archiving. Bio-tropica 42, 399–401

3. Mills, J.A. et al. (2015) Archiving primary data: solutions forlong-term studies. Trends Ecol. Evol. 30, 581–589

4. Roche, D.G. et al. (2014) Troubleshooting public data archiv-ing: suggestions to increase participation. PLoS Biol. 12,e1001779

5. Duke, C.S. and Porter, J.H. (2013) The ethics of data sharingand reuse in biology. Bioscience 63, 483–489

6. Piwowar, H.A. et al. (2011) Data archiving is a good invest-ment. Nature 473, 285

7. Wicherts, J.M. et al. (2011) Willingness to share researchdata is related to the strength of the evidence and the qualityof reporting of statistical results. PLoS ONE 6, e26828

8. Vines, T.H. et al. (2014) The availability of research datadeclines rapidly with article age. Curr. Biol. 24, 94–97

9. Vines, T.H. (2013) Mandated data archiving greatly improvesaccess to research data. FASEB J. 27, 1304–1308

TREE 2035 No. of Pages 3

LetterSolutions forArchiving Data inLong-Term Studies:A Reply toWhitlock et al.James A. Mills,1,53,*Céline Teplitsky,2,3,53

Beatriz Arroyo,4

Anne Charmantier,3

Peter. H. Becker,5

Tim R. Birkhead,6

Pierre Bize,7

Daniel T. Blumstein,8

Christophe Bonenfant,9

Stan Boutin,10

Andrey Bushuev,11

Emmanuelle Cam,12

Andrew Cockburn,13

Steeve D. Côté,14

John C. Coulson,15

Francis Daunt,16

Niels J. Dingemanse,17,18

Blandine Doligez,9

Hugh Drummond,19

Richard H.M. Espie,20

Marco Festa-Bianchet,21

Francesca D. Frentiu,22

John W. Fitzpatrick,23

Robert W. Furness,24

Gilles Gauthier,14

Peter R. Grant,25

Michael Griesser,26

Lars Gustafsson,27

Bengt Hansson,28

Michael P. Harris,16

Frédéric Jiguet,2

Petter Kjellander,29

Erkki Korpimäki,30

Charles J. Krebs,31

Luc Lens,32

John D.C. Linnell,33

Matthew Low,34

Andrew McAdam,35

Antoni Margalida,36

Juha Merilä,37

Anders P. Møller,38

Shinichi Nakagawa,39

Jan-Åke Nilsson,27

Ian C.T. Nisbet,40

Arie J. van Noordwijk,41

Daniel Oro,42 Tomas Pärt,34

Fanie Pelletier,21

Jaime Potti,43 Benoit Pujol,12

Denis Réale,44

Robert F. Rockwell,45

Yan Ropert-Coudert,46

Alexandre Roulin,47

Christophe Thébaud,12

James S. Sedinger,48

Jon E. Swenson,49

Marcel E. Visser,41

Sarah Wanless,16

David F. Westneat,50

Alastair J. Wilson,51 andAndreas Zedrosser52

In our recent paper [1], we discussedsome potential undesirable consequen-ces of public data archiving (PDA) withspecific reference to long-term studiesand proposed solutions to manage theseissues. We reaffirm our commitment todata sharing and collaboration, both ofwhich have been common and fruitfulpractices supported for many decadesby researchers involved in long-termstudies. We acknowledge the potentialbenefits of PDA (e.g., [2]), but believe thatseveral potential negative consequencesfor science have been underestimated [1](see also [3,4]). The objective of ourrecent paper [1] was to define practicesto simultaneously maximize the benefitsandminimize the potential unwanted con-sequences of PDA.

Commenting on our paper, several formerand current editors of major ecology andevolution journals [5] acknowledge the

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need to improve data archiving practicesto account for the concerns presented in[1]. The fact that editors of several journalswere willing to comment on our paperunderlines the importance of this issueand we are keen to continue this dialogueto identify potential solutions. Followingour [1] and Roche et al.’s [6] suggestions,Whitlock et al. [5] endorse as good prac-tice longer embargos (5 years) andencourage cooperation or collaborationwith data providers. Both steps are majoradvances as many of the Principal Inves-tigators (PIs) in [1] have been denied lon-ger embargos, and the practice ofconsulting PIs to ensure that data filesare properly interpreted is not a formalpolicy in any scientific journal.

We welcome these positive developmentsbut underline three concerns, two ofwhich extend beyond the purview of indi-vidual journals.

Whitlock et al. [5] mention that currentpolicies ‘require only that authors makeavailable the data necessary to recreatethe analyses and results in the publishedmanuscript’. For an article that includes ananalysis based on a pedigree and individ-ual data or on lifetime reproductive suc-cess and potential predictor variables, thisrequirement involves providing a detaileddatabase of the breeding performance ofindividuals and their progeny over deca-des. The costs of data gathering, includingresources beyond monetary ones, areborne by the data providers and theirinstitutions not by those who would usethe data; consequently, providing suchextensive datasets is sustainable if thedata are used only to verify the originalanalysis. Extending an embargo to 5 yearsfor such data is a good step, but for stud-ies that extend over decades a longerembargo is warranted, notably to furtherencourage potential users to contacts PIsto get the latest version of the data, andideally collaborate.

Databases from long-term studies are anevolving infrastructure that underpins

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TREE 2035 No. of Pages 3

numerous publications. New data areadded each year and errors and omis-sions are corrected regularly. Over time,archives often include various versions offragmented datasets that: (i) could becombined by others in ways that the datacollectors were already doing or planningto do themselves; or (ii) may differ fromeach other in ways that are likely to lead tomisinterpretation of the data. A single jour-nal's PDA policy cannot ensure that datafrom long-term studies are not misused. Itmust be a community decision. Somepotential solutions include archiving atinstitutional servers with separate policiesfor the distribution of data necessary toreproduce previously published analysesand data requests for additional analyses.The additional analyses would require col-laboration with the PI.

Finally, journal editors do not control thepolicies of funding agencies but their stat-ure in the community can be influential.Whitlock et al. [5] suggest that fundersshould set standards for openness. How-ever, long-term studies typically involveseveral grants and multiple funding agen-cies, sometimes from different countries.Hence, any discrepancy between theirpolicies can lead to potentially insolubleconflict. Institutions that fund a significantproportion of the research, potentially overdecades, may also question the value ofcontinued funding if the data are freelyavailable to individuals from otherorganizations.

We are encouraged by the letter fromWhitlock et al. [5], but believe that thereare additional issues that need to beaddressed. Some of these may besolved by a more explicit and flexiblepolicy on longer embargos, data storageon institutional servers, and involvementof the principal investigators in new anal-yses using the data they produced,through collaboration or reviews. Wehope that this important dialogue willcontinue.

2 Trends in Ecology & Evolution, Month Year, Vol. xx, No. y

110527A Skyline Drive, Corning, NY 14830, USA2CESCO, UMR7204 Sorbonne Universités-MNHN-CNRS-

UPMC, CP51, 55 rue Buffon, 75005 Paris, France3Centre d’Ecologie Fonctionnelle et Evolutive UMR 5175,

Campus CNRS, 1919 route de Mende, 34293 Montpellier

Cedex 5, France4Instituto de Investigacion en Recursos Cinegeticos (IREC)

(CSIC-UCLM-JCCM), Ronda de Toledo s/n, 13005

Ciudad, Real, Spain5Institute of Avian Research, “Vogelwarte Helgoland”, An

der Vogelwarte 21 D26386 Wilhelmshaven, Germany6Department of Animal and Plant Sciences, University of

Sheffield, Sheffield, UK7Institute of Biological and Environmental Sciences,

University of Aberdeen, Aberdeen, UK8Department of Ecology and Evolutionary Biology,

University of California, 621 Young Drive South, Los

Angeles, CA 90095-1606, USA9CNRS, Université Lyon 1, Université de Lyon, UMR 5558,

Laboratoire Biométrie et Biologie Évolutive, 43 boulevard

du 11 Novembre 1918, F-69622 Villeurbanne Cedex,

France10Department of Biological Sciences, University of Alberta,

Edmonton, AB T6G 2E9, Canada11Department of Vertebrate Zoology, Faculty of Biology,

Lomonosov Moscow State University, Leninskie Gory 1/

12, 119234 Moscow, Russia12UMR 5174 EDB Laboratoire Évolution et Diversité

Biologique, CNRS, ENFA, Université Toulouse 3 Paul

Sabatier, Toulouse 31062 Cedex 9, France13Department of Evolution, Ecology, and Genetics,

Research School of Biology, The Australian National

University, Canberra, Australia14Département de Biologie and Centre d’Études

Nordiques, Université Laval, 1045 avenue de la Médecine,

QC G1V 0A6, Canada1529St Mary's Close, Shincliffe, Durham DH1 2ND, UK16Centre for Ecology and Hydrology, Bush Estate,

Penicuik EH26 0QB, UK17Behavioural Ecology, Department of Biology, Ludwig

Maximilian University of Munich, Planegg-Martinsried,

Germany18Evolutionary Ecology of Variation Research Group, Max

Planck Institute for Ornithology, Seewiesen, Germany19Departamento de Ecología Evolutiva, Instituto de

Ecología, Universidad Nacional Autónoma de México, AP

70-275, México DF 04510, México20Technical Resource Branch, Saskatchewan Ministry of

Environment, 3211 Albert Street, Regina, SK S4S 5W6,

Canada21Département de Biologie, Université de Sherbrooke,

2500 boulevard de L’Université, Sherbrooke, QC J1K 2R1,

Canada22School of Biomedical Sciences and Institute of Health

and Biomedical Innovation, Queensland University of

Technology, Kelvin Grove, QLD 4059, Australia23Cornell Laboratory of Ornithology, 159 Sapsucker

Woods Road, Ithaca, NY 14850, USA24Graham Kerr Building, University of Glasgow, Glasgow

G12 8QQ, UK25Department of Ecology and Evolutionary Biology,

Princeton University, Princeton, NJ 08544-1003, USA26Anthropological Institute and Museum, University of

Zürich, Zürich, Switzerland27Department of Animal Ecology, Evolutionary Biology

Center, Uppsala University, Uppsala, Sweden

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28Department of Biology, Lund University, Ecology

Building, 223 62 Lund, Sweden29Grimso Wildlife Research Station, Department of

Ecology, Swedish University of Agricultural Sciences

(SLU), SE-73091 Riddarhyttan, Sweden30Section of Ecology, Department of Biology, University of

Turku, FI-20014 Turku, Finland31Department of Zoology, University of British Columbia,

Vancouver, BC V6T 1Z4, Canada32Terrestrial Ecology Unit, Department of Biology, Ghent

University, Ledeganckstraat 35, B-9000 Gent, Belgium33Norwegian Institute for Nature Research, PO Box 5685

Sluppen, N-7485 Trondheim, Norway34Department of Ecology, Swedish University of

Agricultural Sciences, 75007 Uppsala, Sweden35Department of Integrative Biology, University of Guelph,

Guelph, ON N1G 2W1, Canada36Faculty of Life Sciences and Engineering, University of

Lleida, E-25198 Lleida, Spain37Ecological Genetics Research Unit, Department of

Biosciences, PO Box 65 (Biocenter 3, Viikinkaari 1), FIN-

00014 University of Helsinki, Finland38Laboratoire Ecologie, Systématique, et Evolution, Equipe

Diversité, Ecologie et Evolution Microbiennes, Bâtiment

362, 91405 Orsay Cedex, France39Evolution and Ecology Research Centre and School of

Biological, Earth, and Environmental Sciences, University

of New South Wales, Sydney, Australia40ICT Nisbet & Company, 150 Alder Lane, North Falmouth,

MA 02556, USA41Department of Animal Ecology, Netherlands Institute of

Ecology (NIOO-KNAW), PO Box 50, 6700 AB Wageningen,

The Netherlands42Institut Mediterrani d’Estudis Avançats IMEDEA (CSIC-

UIB), Miquel Marques 21, 07190 Esporles Mallorca, Spain43Departamento de Ecologia Evolutiva, Estación Biológica

de Doñana-CSIC, Av. Américo Vespucio s/n, 41092

Seville, Spain44Département des Sciences Biologiques, Université du

Québec à Montréal, CP 8888-succursale Centre-Ville,

Montreal, QC H3C 3P8, Canada45Vertebrate Zoology, American Museum of Natural

History, New York, NY 10024, USA46Institut Pluridisciplinaire Hubert Curien, CNRS UMR7178,

23 rue Becquerel, 67087 Strasbourg, France47Department of Ecology and Evolution, University of

Lausanne, Lausanne, Switzerland48Department of Natural Resources and Environmental

Science, University of Nevada Reno, Reno, NV 89512,

USA49Department of Ecology and Natural Resource

Management, Norwegian University of Life Sciences, PO

Box 5003, NO-1432 Ås, Norway and Norwegian Institute

for Nature Research, PO Box 5685 Sluppen, N-7485

Trondheim, Norway50Department of Biology, Center for Ecology, Evolution,

and Behavior, University of Kentucky, Lexington, KY, USA51Centre for Ecology and Conservation, College of Life

and Environmental Sciences, University of Exeter,

Cornwall Campus, Penryn TR10 9EZ, UK52Faculty of Arts and Sciences, Department of

Environmental and Health Studies, Telemark University

College, N-3800 Bø i Telemark, Norway53These authors contributed equally

TREE 2035 No. of Pages 3

*Correspondence: dmills@stny.rr.com (J.A. Mills).

http://dx.doi.org/10.1016/j.tree.2015.12.004

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long-term studies. Trends Ecol. Evol. 30, 581–589

2. Moore, A.J. et al. (2010) The need for archiving data inevolutionary biology. J. Evol. Biol. 23, 659–660

3. Katzner, T. (2015) Do open access data policies inhibitinnovation? Bioscience 65, 1037–1038

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