comment COVID-19 lockdown allows researchers to quantify the efects of human activity on wildlife Reduced human mobility during the pandemic will reveal critical aspects of our impact on animals, providing important guidance on how best to share space on this crowded planet. Christian Rutz, Matthias-Claudio Loretto, Amanda E. Bates, Sarah C. Davidson, Carlos M. Duarte, Walter Jetz, Mark Johnson, Akiko Kato, Roland Kays, Thomas Mueller, Richard B. Primack, Yan Ropert-Coudert, Marlee A. Tucker, Martin Wikelski and Francesca Cagnacci

ver the past few months, many Unprecedented circumstances countries around the world went Box 1 | Introducing ‘anthropause’ As expanding human populations Ointo lockdown to control the are transforming environments at spread of COVID-19. Brought about by the We noticed that people started referring to unprecedented rates, understanding the most tragic circumstances, this period of the lockdown period as the ‘Great Pause’, linkages between human and animal unusually reduced human mobility — which but felt that a more precise term would behaviour is of critical importance. It is we suggest be coined ‘anthropause’ (see be helpful. We propose ‘anthropause’ to key to preserving global biodiversity, to Box 1) — may provide important insights refer specifcally to a considerable global maintaining the integrity of ecosystems, into human–wildlife interactions in the slowing of modern human activities, and to predicting global zoonoses and twenty-first century. Anecdotal observations notably travel. We are aware that the environmental change5. This knowledge is indicate that many animal species are correct prefx is ‘anthropo-’ (for ‘human’) not only worth billions of dollars, but it is enjoying the newly afforded peace and quiet, but opted for the shortened form, which also vital for shaping a sustainable future. while others, surprisingly, seem to have is easier to remember and use, and where So far, however, researchers have had come under increased pressure. the missing ‘po’ is still echoed in the to rely predominantly on purely Here, we highlight how the pronunciation of ‘pause’ (pɔːz). observational approaches. international research community can Scientists have long sought to quantify use these extraordinary circumstances how humans impact various aspects of to gain unprecedented mechanistic following reductions in vessel traffic and animal biology, such as population levels, insight into how human activity affects noise-pollution levels1. reproductive and mortality rates, movement wildlife. We outline urgent steps different But for some species, the pandemic may and activity patterns, foraging behaviour, stakeholder groups need to take to ensure have created new challenges. For example, and stress responses1,6–8. Studies usually this opportunity is not missed, and various urban-dwelling animals, like rats, employ one of two main approaches — introduce global collaborative research gulls or monkeys, have become so reliant on spatial comparisons or temporal analyses. initiatives that are currently forming food discarded or provided by humans that The first involves comparing a species’ to facilitate coordination. Scientific they may struggle to make ends meet under biology across areas that differ in human knowledge gained during this devastating current conditions. Interestingly, in some activity. Such differences occur, for example, crisis will allow us to develop innovative countries where lockdowns allow outdoor along urban gradients, with increasing strategies for sharing space on this exercise, humans are flocking to green distance from coastlines, or between increasingly crowded planet, with benefits spaces in or near metropolitan areas (see protected and unprotected areas. The second for both wildlife and humans. Fig. 1), potentially disturbing resident approach documents how animals respond wildlife2. At the same time, reduced to temporal changes in human activity in Possible efects on wildlife human presence in more remote areas may a given locality, which may be short-term6 Social media abound with posts sharing potentially expose endangered species, such (for example, holiday periods, or natural surprising wildlife encounters during as rhinos or raptors, to increased risk of or human-made disasters) or longer-term lockdown. As we gaze out of our windows, poaching or persecution3. Finally, concerns (for example, changes in protection status, or relish a brief walk in the park, nature have been raised that, in low-income or land- or seascape modification through appears to have changed, especially in urban countries, economic hardship may force construction). environments. There not only seem to be increased exploitation of natural resources4. The reduction in human mobility on more animals than usual, but there are At present, it is impossible to say which land and at sea during the anthropause is also some unexpected visitors. People have observations have been hyped by social unparalleled in recent history9,10. Lockdown reported sightings of pumas in downtown media, and which expert predictions about effects have been drastic, sudden, and Santiago, Chile, of dolphins in untypically global animal responses will hold true. But widespread. Countries have also responded calm waters in the harbour of Trieste, what is clear is that humans and wildlife in broadly similar ways across large parts of Italy, and of jackals in broad daylight in have become more interdependent than ever the world, presenting invaluable replicates urban parks in Tel Aviv, Israel. Hidden before, and that now is the time to study of this perturbation. So, how exactly can from view, animals may also start roaming this complex relationship. A quantitative we make the most of these exceptional more freely across the world’s oceans, scientific investigation is urgently needed. circumstances?

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While every field study has value in its own right, the pandemic affords an opportunity to build a global picture of animal responses by pooling large numbers of datasets. Such collaborative projects can integrate the spatial and temporal approaches outlined above, in an attempt to uncover causal relationships. Aspects of animals’ biology can be compared Humans per km2 across sites that vary in COVID-19-related 0 26 to 250 1 251 to 1,000 restrictions and resultant changes in human 2 to 5 >1,000 mobility, and across different time periods, 6 to 25 spanning from before until after changes Subsample of bio-logging studies occurred. Taking into account additional Avian data from unaffected ‘control’ sites11, such Marine as particularly remote or inaccessible areas, Terrestrial researchers will be able to examine if, and how, animals responded to reductions in human activity. Baseline data from similar time periods in prior years, and from years following the COVID-19 pandemic, will considerably strengthen inferences, helping to disentangle anthropause effects from natural seasonal variation in animal biology. Finally, we wish to share a very important sentiment. While this is no doubt a valuable research opportunity, it is one that has only come about through tragic circumstances. % change in humans visiting parks Scientists who prepare to study lockdown No data 1 to 25 effects on wildlife, and on the environment –100 to –76 26 to 50 more generally, should be sensitive to –75 to –51 51 to 75 the immense human suffering caused by –50 to –26 76 to 100 –25 to –1 >100 COVID-19 and use appropriate language to 0 describe their work.

Mobilizing the community Fig. 1 | Illustrating the research potential of the recently launched COVID-19 Bio-Logging Initiative. Top: locations of a subsample of active animal tracking (‘bio-logging’) studies superimposed on human General insights about animal responses — population density. Data sources: 801 publicly visible animal tracking studies from the Movebank across different species, geographic regions, research platform (www.movebank.org) that are likely to contain data overlapping with the COVID-19 ecosystems, and levels of human activity period (data extracted 18 May 2020). ‘Marine’ includes seabirds and other marine species, ‘avian’ — will only be possible if researchers pool refers to all other bird species, and ‘terrestrial’ are non-avian species living mostly on land. Population their data and expertise. Several initiatives density data sourced from ref. 15 (data accessed 15 May 2020). Bottom: median percentage of change are busy preparing global-scale collaborative based on daily values (with reference to the data provider’s default baseline from the five-week period research projects to achieve exactly this. between 3 January and 6 February 2020) in visits to places like local parks, national parks, public One of them — the COVID-19 beaches, marinas, dog parks, plazas and public gardens for the month of April 2020. Data are plotted Bio-Logging Initiative (www.bio-logging. for 900 subregions within 131 countries (note that for 1.6% of the subregions fewer than 5 daily values net) — recently formed under the umbrella were available for April 2020). This information should be interpreted cautiously, and is shown here of the International Bio-Logging Society, in merely to provide a preliminary, coarse-scale illustration of some recent changes in human mobility; collaboration with the Movebank research scientific analyses will require higher-resolution, calibrated data. Data sourced from ref. 16 (data platform, and the Max Planck–Yale Center accessed 7 May 2020). Both maps were drawn with the QGIS Geographic Information System for Biodiversity Movement and Global (http://qgis.org), using freely available data (2018) for country borders from GADM Change. This large consortium is planning (https://gadm.org) (data accessed 6 May 2020). to use data collected by ‘bio-loggers’ — miniature, animal-attached electronic devices — to measure changes in animals’ movement, behaviour, activity and physiology, as well as in the environments with new data from the anthropause, to mobility and activity on species and they inhabit (see Fig. 1). The project address a previously intractable question: ecosystems by integrating a wide array of considers all species for which owners are the movements of animals in modern information, including data generated by are willing to contribute data, and has landscapes predominantly affected by species monitoring programmes, protected already received enthusiastic support built structures, or by the presence of area networks, sensor networks and citizen from both the marine and the terrestrial humans? science initiatives. Several additional bio-logging research communities. As Another initiative — led by the projects are forming at pace. their first objective, the team will update PAN-Environment working group — is These initiatives provide valuable an earlier study on terrestrial mammals8 planning to assess impacts of human platforms for wildlife biologists, human

Nature Ecology & Evolution | www.nature.com/natecolevol comment mobility researchers, bioinformaticians and relevant stakeholders — including wildlife major benefits for ecosystems and humans. other experts, to join forces for ambitious researchers, owners of high-quality For example, small modifications to the large-scale analyses. This crisis, and the human mobility data, experts on data topology and operation of our transport unique research opportunities it affords, confidentiality, and legislators — to form networks may drastically reduce unintended demand such collaboration, as well as full partnerships that facilitate investigations disruptive effects on animal movement. transparency and effective coordination. of anthropause impacts at the highest Coordinated global wildlife research possible spatio-temporal resolution, in full during the anthropause will make Urgent steps compliance with the law13. contributions that go well beyond informing Immediate action is required from a range Finally, additional funding is urgently conservation science — it will challenge of stakeholder groups to ensure that we required to support the research programme humanity to reconsider our future on Earth. maximize the scientific insight that arises we envision. This includes funds for field There will be unforeseen opportunities from this devastating pandemic. Here are data collection, for data-management to reinvent the way we live our lives, and some practical recommendations for the infrastructure and support, and for complex to forge a mutually beneficial coexistence short- to mid-term. data analyses. We know that follow-on with other species. It would be wonderful if First of all, it is of paramount importance field studies are not normally considered careful research during this period of crisis that field biologists can continue with a priority by funding agencies, but these helped us to find innovative ways of reining data collection even under lockdown are precisely the kinds of projects that can in our increasingly expansive lifestyles, conditions2,10,12, with appropriate safety now contribute critically important data to rediscover how important a healthy precautions. The analyses we outlined series. Field projects must continue data environment is for our own well-being, and above depend on high-quality data, which collection during the ups and downs in to replace a sense of owning with a sense means a wide range of activities must carry human mobility we will likely witness over of belonging5,14. We hope that people will on unhindered, such as instrumenting the coming months and beyond. choose to hear the wake-up call. ❐ animals with bio-loggers, servicing of field We do not advocate diverting resources equipment (for example, camera traps or from front-line work or ongoing research on Christian Rutz 1,2 ✉ , receiver stations), and conducting routine vaccines, diagnostic tests and therapeutics — Matthias-Claudio Loretto 3,4, surveys. Local authorities and research funds for human–wildlife interactions must Amanda E. Bates 5, institutions should swiftly issue the come from separate parts of governmental Sarah C. Davidson 3,6, Carlos M. Duarte 7, required permits12. budgets that are concerned more broadly Walter Jetz 8,9, Mark Johnson10,11, We are confident that researchers will be with human and environmental health. Akiko Kato12, Roland Kays13,14, keen to resume fieldwork, but recommend Some governments have started working on Thomas Mueller15,16, Richard B. Primack17, they take a few extra steps. First, we such schemes. Yan Ropert-Coudert 12, suggest they keep detailed records of Marlee A. Tucker 18, Martin Wikelski3,6 and official restrictions on (and where possible, A post-anthropause world Francesca Cagnacci19 observed changes in) human mobility in Society’s priority must be to tackle the 1Centre for Biological Diversity, School of Biology, their study areas, as this information may immense human tragedy and hardship University of St Andrews, St Andrews, UK. be difficult to reconstruct after the fact. caused by COVID-19. But we cannot afford 2Radclife Institute for Advanced Study, Harvard While measures of human activity can to miss the opportunity to chart — for the University, Cambridge, MA, USA. 3Department be obtained from a variety of ‘big data’ first time on a global scale — the extent of Migration, Max Planck Institute of Animal sources, field observations are required to which modern human mobility Behavior, Radolfzell, Germany. 4Department of for validation. Second, we encourage the affects wildlife9. Biology, University of Konstanz, Konstanz, Germany. leaders of local projects to get in touch as So, what do we hope to learn? Research 5Department of Ocean Sciences, Memorial University soon as possible with the larger collaborative on anthropause effects will enable a detailed, of Newfoundland, St. John’s, Newfoundland, initiatives that are being launched, to enable mechanistic understanding of human– Canada. 6Centre for the Advanced Study of data standardization, exchange of expertise wildlife interactions. It will help us identify Collective Behaviour, University of Konstanz, and coordination. Contribution to these species that are seriously affected by human Konstanz, Germany. 7Red Sea Research Center and initiatives does not preclude independent activity, yet still have the capacity to respond Computational Biosciences Research Center, King research outputs, but is essential for to change, as well as others that appear Abdullah University of Science and Technology, global-scale analyses. particularly vulnerable. It will also reveal Tuwal, Kingdom of Saudi Arabia. 8Ecology and Researchers seeking to measure human critical thresholds beyond which human Evolutionary Biology Department, Yale University, impact on wildlife often face a frustrating disturbance has detrimental effects on New Haven, CT, USA. 9Center for Biodiversity and dilemma — they have high-quality data animal behaviour, species persistence and Global Change, Yale University, New Haven, CT, for their study animals, but only crude ecosystem dynamics, helping us pinpoint USA. 10Sea Mammal Research Unit, University of St proxies of human activity. Studies have processes that negatively feedback on human Andrews, St Andrews, UK. 11Department of Biology, used land-cover data, proximity to roads well-being5. Aarhus University, Aarhus, Denmark. 12Centre or settlements, or fishing vessels’ radar These insights will inspire realistic, d’Etudes Biologiques de Chizé, La Rochelle Université signals, to make inferences about human evidence-based proposals for improving − CNRS, UMR 7372, Villiers en Bois, France. 13North disturbance8. These metrics usually offer human–wildlife coexistence. Nobody is Carolina Museum of Natural Sciences, Biodiversity reasonable approximations, but in situ asking for humans to remain in a state of Lab, Raleigh, NC, USA. 14Fisheries, Wildlife, and measurements — such as GPS tracking permanent lockdown. The COVID-19 Conservation Biology Program, College of Natural logs from mobile phones, traffic-flow anthropause has transported us back to Resources, North Carolina State University, Raleigh, measurements on land and at sea, and levels of human mobility observed a few NC, USA. 15Senckenberg Biodiversity and Climate high-resolution satellite images — are decades — not centuries — ago. That means Research Centre, Senckenberg Gesellschaf für required to capture the rapidly changing that we may discover that relatively minor Naturforschung, Frankfurt (Main), Germany. conditions under lockdown. We urge changes to our lifestyles can potentially have 16Department of Biological Sciences, Goethe

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University, Frankfurt (Main), Germany. 17Biology 5. Cook, R. A., Karesh, W. B. & Osofsky, S. A. Te Manhattan Acknowledgements Principles on ‘One World, One Health’ (Wildlife Conservation Department, Boston University, Boston, MA, USA. Manuscript preparation was supported through: a Radcliffe Society, 2004). Fellowship at the Radcliffe Institute for Advanced Study, 18Department of Environmental Science, Institute for 6. Larson, C. L., Reed, S. E., Merenlender, A. M. & Crooks, K. R. Harvard University (to C.R.); the European Union’s PLoS ONE 11, e0167259 (2016). Water and Wetland Research, Radboud University, Horizon 2020 research and innovation programme under 19 7. Gaynor, K. M., Hojnowski, C. E., Carter, N. H. & Brashares, J. S. Nijmegen, Te Netherlands. Department of Science 360, 1232–1235 (2018). the Marie Skłodowska-Curie grant agreement no. 798091 Biodiversity and Molecular Ecology, Research and 8. Tucker, M. A. et al. Science 359, 466–469 (2018). (to M.-C.L.); and Autonomous Province of Trento ordinary Innovation Centre, Fondazione Edmund Mach, 9. Rosenbloom, D. & Markard, J. Science 368, 447 (2020). funds to Fondazione Edmund Mach (to F.C.). 10. Saraswat, R. & Saraswat, D. A. Science 368, 594–595 (2020). Trento, Italy. 11. Christie, A. P. et al. J. Appl. Ecol. 56, 2742–2754 (2019). Author contributions ✉ e-mail: [email protected] 12. Inouye, D. W., Underwood, N., Inouye, B. D. & Irwin, R. E. The idea for this Comment was conceived by the COVID- Science 368, 724–725 (2020). 19 Bio-Logging Initiative. C.R., M.-C.L. and F.C. initiated Published: xx xx xxxx 13. Oliver, N. et al. Sci. Adv. 6, eabc0764 (2020). and coordinated manuscript preparation; C.R. drafted 14. Mace, G. M. Science 345, 1558–1560 (2014). the manuscript with contributions from M.-C.L. and F.C.; https://doi.org/10.1038/s41559-020-1237-z 15. Center For International Earth Science Information Network M.-C.L. prepared the figure; S.C.D. extracted bio-logging (CIESIN), Columbia University Gridded Population of the World, data from Movebank; and all authors provided critical References version 4 (GPWv4): Population Density Adjusted to Match 2015 1. Jones, N. Nature 568, 158–161 (2019). Revision UN WPP Country Totals, Revision 11 (2018) (NASA feedback on a draft. Apart from the three lead authors (C.R., 2. Corlett, R. T. et al. Biol. Conserv. 246, 108571 (2020). Socioeconomic Data and Applications Center (SEDAC), accessed M.-C.L. and F.C.), all co-authors are listed alphabetically. 3. Buckley, R. Biol. Conserv. 247, 108640 (2020). 15 May 2020); https://doi.org/10.7927/H4F47M65 4. Gardner, C. Nature’s comeback? No, the coronavirus pandemic 16. Google COVID-19 Community Mobility Reports (Google LLC, Competing interests threatens the world’s wildlife. Te Conversation (14 April 2020). accessed 7 May 2020); https://www.google.com/covid19/mobility/ The authors declare no competing interests.

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