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Unexpected diversity in socially synchronized rhythms of shorebirds

View ORCID ProfileMartin Bulla, Mihai Valcu, Adriaan M. Dokter, Alexei G. Dondua, András Kosztolányi, Anne Rutten, Barbara Helm, Brett K. Sandercock, Bruce Casler, Bruno J. Ens, Caleb S. Spiegel, Chris J. Hassell, Clemens Küpper, Clive Minton, Daniel Burgas, David B. Lank, David C. Payer, Egor Y. Loktinov, Erica Nol, Eunbi Kwon, Fletcher Smith, H. River Gates, Hana Vitnerová, Hanna Prüter, James A. Johnson, James J. H. St Clair, Jean-François Lamarre, Jennie Rausch, Jeroen Reneerkens, Jesse R. Conklin, Joana Burger, Joe Liebezeit, Joël Bêty, Jonathan T. Coleman, Jordi Figuerola, Jos C. E. W. Hooijmeijer, José A. Alves, Joseph A. M. Smith, Karel Weidinger, Kari Koivula, Ken Gosbell, Klaus-Michael Exo, Larry Niles, Laura Koloski, Laura McKinnon, Libor Praus, Marcel Klaassen, Marie-Andrée Giroux, Martin Sládeček, Megan L. Boldenow, Michael I. Goldstein, Miroslav šálek, Nathan Senner, Nelli Rönkä, Nicolas Lecomte, Olivier Gilg, Orsolya Vincze, Oscar W. Johnson, Paul A. Smith, Paul F. Woodard, Pavel S. Tomkovich, Phil F. Battley, Rebecca Bentzen, Richard B. Lanctot, Ron Porter, Sarah T. Saalfeld, Scott Freeman, Stephen C. Brown, Stephen Yezerinac, Tamás Székely, Tomás Montalvo, Theunis Piersma, Vanessa Loverti, Veli-Matti Pakanen, Wim Tijsen, Bart Kempenaers
doi: https://doi.org/10.1101/084806
Martin Bulla
1Department of Behavioural Ecology and Evolutionary Genetics, Max Planck Institute for Ornithology, Eberhard Gwinner Str, 82319 Seewiesen, Germany
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  • ORCID record for Martin Bulla
Mihai Valcu
1Department of Behavioural Ecology and Evolutionary Genetics, Max Planck Institute for Ornithology, Eberhard Gwinner Str, 82319 Seewiesen, Germany
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Adriaan M. Dokter
2Computational Geo-Ecology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Science Park 904, 1098 XH, Amsterdam, The Netherlands
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Alexei G. Dondua
3Gatchinskaya, apartment 27, St-Petersburg 197198, Russia
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András Kosztolányi
4Department of Ecology, University of Veterinary Medicine Budapest, Rottenbiller u. 50., Budapest H-1077, Hungary
5MTA-DE “Lendület” Behavioural Ecology Research Group, Department of Evolutionary Zoology, University of Debrecen, Egyetem tér 1., Debrecen H-4032, Hungary
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Anne Rutten
1Department of Behavioural Ecology and Evolutionary Genetics, Max Planck Institute for Ornithology, Eberhard Gwinner Str, 82319 Seewiesen, Germany
6Apiloa GmbH, Starnberg 82319, Germany
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Barbara Helm
7Institute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, Graham Kerr Building, Glasgow G12 8QQ, UK
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Brett K. Sandercock
8Division of Biology, Kansas State University, 116 Ackert Hall, Manhattan, Kansas 66506-4901, USA
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Bruce Casler
9PO Box 1094, Fallon, Nevada 89407, USA
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Bruno J. Ens
10Coastal Ecology Team, Sovon Dutch Centre for Field Ornithology, PO Box 59, Den Burg 1790 AB, Texel, The Netherlands
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Caleb S. Spiegel
11Division of Migratory Birds, Northeast Region, US Fish and Wildlife Service, 300 Westgate Center Dr, Hadley, Massachusetts 01035, USA
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Chris J. Hassell
12Global Flyway Network, PO Box 3089, Broome, Western Australia 6725, Australia
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Clemens Küpper
13Institute of Zoology, University of Graz, Universitätsplatz 2, 8010 Graz, Austria
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Clive Minton
14Victorian Wader Study group, 165 Dalgetty Road, Beaumaris, Melbourne, Victoria 3193, Australia
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Daniel Burgas
15Department of Forest Sciences, University of Helsinki, PO Box 27, Helsinki FI-00014, Finland
16Department of Biological and Environmental Sciences, University of Jyväskylä, PO Box 35, Jyväskylä FI-40014, Finland
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David B. Lank
17Department of Biological Sciences, Simon Fraser University, 8888 University Drive, Burnaby, British Columbia V5A 1S6, Canada
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18Alaska Region, US National Park Service, 240 W 5th Ave, Anchorage, Alaska 99501, USA
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19State Lab for Photon Energetics, Bauman Moscow State Technical University, 2nd Baumanskaya St, 5-1, Moscow 105005, Russia
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20Biology Department, Trent University, 2140 East Bank Drive, Peterborough, Ontario K9L 0G2, Canada
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21Department of Fish and Wildlife Conservation, Virginia Polytechnic Institute and State University, 310 West Campus Drive, Blacksburg, Virginia 24061, USA
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Fletcher Smith
22Center for Conservation Biology, College of William & Mary and Virginia Commonwealth University, PO Box 8795, Williamsburg, Virginia 23187, USA
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H. River Gates
23Pacifica Ecological Services, 17520 Snow Crest Lane, Anchorage, Alaska 99516, USA
24Migratory Bird Management, US Fish and Wildlife Service, 1011 East Tudor Road, Anchorage, Alaska 99503, USA
25Shorebird Recovery Program, Manomet, PO Box 545, Saxtons River, Vermont 05154, USA
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26Faculty of Science, Charles University in Prague, Albertov 6, Praha 128 43, Czech Republic
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Hanna Prüter
27Department of Wildlife Diseases, Leibniz Institute for Zooand Wildlife Research, Alfred-Kowalke-Straβe 17, Berlin 10315, Germany
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James A. Johnson
24Migratory Bird Management, US Fish and Wildlife Service, 1011 East Tudor Road, Anchorage, Alaska 99503, USA
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James J. H. St Clair
28Biodiversity Lab, Department of Biology and Biochemistry, University of Bath, Claverton Down, Bath BA1 7AY, UK
29Centre for Evolutionary Biology, School of Biology, University of Western Australia, Stirling Highway, Crawley, Western Australia 6009, Australia
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Jean-François Lamarre
30Département de biologie, chimie et géographie and Centre d’études nordiques (CEN), Université du Québec à Rimouski, 300 allée des Ursulines, Rimouski, Quebec G5L 3A1, Canada
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31Canadian Wildlife Service, Environment and Climate Change Canada, PO Box 2310, 5019–-52nd Street, 4th Floor, Yellowknife, Northwest Territories X1A 2P7, Canada
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Jeroen Reneerkens
32Conservation Ecology Group, Groningen Institute for Evolutionary Life Sciences, University of Groningen, Nijenborgh 7, Groningen 9747 AG, The Netherlands
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Jesse R. Conklin
32Conservation Ecology Group, Groningen Institute for Evolutionary Life Sciences, University of Groningen, Nijenborgh 7, Groningen 9747 AG, The Netherlands
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33Division of Life Sciences, Rutgers University, 604-Allison Road, Piscataway, New Jersey 08854-8082, USA
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34Audubon Society of Portland, 5151 NW Cornell Road, Portland, Oregon 97210, USA
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30Département de biologie, chimie et géographie and Centre d’études nordiques (CEN), Université du Québec à Rimouski, 300 allée des Ursulines, Rimouski, Quebec G5L 3A1, Canada
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35Queensland Wader Study Group, 22 Parker Street, Brisbane, Queensland 4128, Australia
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Jordi Figuerola
36Department of Wetland Ecology, Doñana Biological Station (CSIC), Av. Américo Vespucio, s/n, Seville 41092, Spain
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32Conservation Ecology Group, Groningen Institute for Evolutionary Life Sciences, University of Groningen, Nijenborgh 7, Groningen 9747 AG, The Netherlands
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José A. Alves
37Centre for Environmental and Marine Studies (CESAM), Department of Biology, University of Aveiro, Campus de Santiago, Aveiro 3810-193, Portugal
38South Iceland Research Centre, University of Iceland, Fjolheimar, Selfoss 800, Iceland
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39LJ Niles Associates, PO Box 784, Cape May, New Jersey 08204, USA
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40Department of Zoology and Laboratory of Ornithology, PalackÝ University, 17. Listopadu 50, Olomouc 771 46, Czech Republic
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41Department of Ecology, University of Oulu, PO Box 3000, Oulu 90014, Finland
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42Australasian Wader Studies Group, 1/19 Baldwin Road, Blackburn, Melbourne, Victoria 3130, Australia
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43Institute of Avian Research, Vogelwarte Helgoland, An der Vogelwarte 21, Wilhelmshaven D-26386, Germany
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44LJ Niles Associates, 109 Market Lane, Greenwich, Connecticut 08323, USA
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45Environmental and Life Sciences, Trent University, 1600 West Bank Dr, Peterborough, Ontario K0L 0G2, Canada
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46Bilingual Biology Program, York University Glendon Campus, 2275 Bayview Avenue, Toronto, Ontario M4N 3M6, Canada
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40Department of Zoology and Laboratory of Ornithology, PalackÝ University, 17. Listopadu 50, Olomouc 771 46, Czech Republic
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47Centre for Integrative Ecology, Deakin University, 75 Pigdons Road, Waurn Ponds, Geelong, Victoria 3216, Australia
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Marie-Andrée Giroux
48Canada Research in Northern Biodiversity and Centre d’Études Nordiques, Université du Québec à Rimouski, 300, Allée des Ursulines, Rimouski, Quebec G5L 3A8, Canada
49Canada Research in Polar and Boreal Ecology and Centre d’Études Nordiques, Université de Moncton, 18 avenue Antonine-Maillet, Moncton, New Brunswick E4K 1A6, Canada
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50Faculty of Environmental Sciences, Czech University of Life Sciences Prague, KamÝcká 1176, Suchdol, Prague 16521, Czech Republic
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51Department of Biology and Wildlife, University of Alaska Fairbanks, PO Box 756100, Fairbanks, Alaska 99775-6100, USA
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Michael I. Goldstein
52Alaska Coastal Rainforest Center, University of Alaska Southeast, 11120 Glacier Hwy, Juneau, Alaska 99801, USA
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Miroslav šálek
50Faculty of Environmental Sciences, Czech University of Life Sciences Prague, KamÝcká 1176, Suchdol, Prague 16521, Czech Republic
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Nathan Senner
32Conservation Ecology Group, Groningen Institute for Evolutionary Life Sciences, University of Groningen, Nijenborgh 7, Groningen 9747 AG, The Netherlands
53Cornell Lab of Ornithology, 159 Sapsucker Woods Road, Ithaca 14850, USA
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41Department of Ecology, University of Oulu, PO Box 3000, Oulu 90014, Finland
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49Canada Research in Polar and Boreal Ecology and Centre d’Études Nordiques, Université de Moncton, 18 avenue Antonine-Maillet, Moncton, New Brunswick E4K 1A6, Canada
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54Equipe Ecologie Evolution, UMR 6282 Biogéosciences, Université de Bourgogne Franche Comté, 6 Bd Gabriel, Dijon 21000, France
55Groupe de Recherche en Ecologie Arctique, 16 Rue de Vernot, Francheville 21440, France
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Orsolya Vincze
5MTA-DE “Lendület” Behavioural Ecology Research Group, Department of Evolutionary Zoology, University of Debrecen, Egyetem tér 1., Debrecen H-4032, Hungary
56Evolutionary Ecology Group, Hungarian Department of Biology and Ecology, Babes,-Bolyai University, Clinicilor 5-7, Cluj-Napoca RO-400006, Romania
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57Department of Ecology, Montana State University, Bozeman, Montana 59717, USA
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58Wildlife Research Division, Environment and Climate Change Canada, 1125 Colonel By Dr, Ottawa, Ontario K1A 0H3, Canada
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31Canadian Wildlife Service, Environment and Climate Change Canada, PO Box 2310, 5019–-52nd Street, 4th Floor, Yellowknife, Northwest Territories X1A 2P7, Canada
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59Zoological Museum, Lomonosov Moscow State University, Bolshaya Nikitskaya St, 6, Moscow 125009, Russia
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Phil F. Battley
60Institute of Agriculture & Environment, Massey University, Private Bag 11 222, Palmerston North 4442, New Zealand
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Rebecca Bentzen
61Arctic Beringia Program, Wildlife Conservation Society, 925 Schloesser Dr, Fairbanks, Alaska 99709, USA
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Richard B. Lanctot
24Migratory Bird Management, US Fish and Wildlife Service, 1011 East Tudor Road, Anchorage, Alaska 99503, USA
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Ron Porter
62Delaware Bay Shorebird Project, Ambler, Pennsylvania 19002, USA
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Sarah T. Saalfeld
24Migratory Bird Management, US Fish and Wildlife Service, 1011 East Tudor Road, Anchorage, Alaska 99503, USA
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Scott Freeman
63Arctic National Wildlife Refuge, US Fish and Wildlife Service, 101 12th Ave, Fairbanks, Alaska 99701, USA
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Stephen C. Brown
25Shorebird Recovery Program, Manomet, PO Box 545, Saxtons River, Vermont 05154, USA
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Stephen Yezerinac
64Fieldday Consulting, Surrey, British Columbia V4N 6M5, Canada
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Tamás Székely
65Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, Claverton Down, Bath BA2 7AY, UK
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Tomás Montalvo
66Servei de Vigilància i Control de Plagues Urbanes, Agència de Salut Pública de Barcelona, Av. Pr­ncep d’Astúries 63, Barcelona 8012, Spain
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Theunis Piersma
32Conservation Ecology Group, Groningen Institute for Evolutionary Life Sciences, University of Groningen, Nijenborgh 7, Groningen 9747 AG, The Netherlands
67NIOZ Royal Netherlands Institute for Sea Research, Department of Coastal Systems and Utrecht University, PO Box 59, Den Burg 1790 AB, Texel, The Netherlands
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Vanessa Loverti
68Migratory Bird and Habitat Program, US Fish and Wildlife Service, 911 NE 11th Avenue, Portland, Oregon 97232, USA
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Veli-Matti Pakanen
41Department of Ecology, University of Oulu, PO Box 3000, Oulu 90014, Finland
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Wim Tijsen
69Poelweg 12, Westerland 1778 KB, The Netherlands
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Bart Kempenaers
1Department of Behavioural Ecology and Evolutionary Genetics, Max Planck Institute for Ornithology, Eberhard Gwinner Str, 82319 Seewiesen, Germany
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  • Abstract
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Abstract

The behavioural rhythms of organisms are thought to be under strong selection, influenced by the rhythmicity of the environment1–4. Such behavioural rhythms are well studied in isolated individuals under laboratory conditions1,5, but free-living individuals have to temporally synchronize their activities with those of others, including potential mates, competitors, prey and predators6–10. Individuals can temporally segregate their daily activities (e.g. prey avoiding predators, subordinates avoiding dominants) or synchronize their activities (e.g. group foraging, communal defence, pairs reproducing or caring for offspring)6–9,11. The behavioural rhythms that emerge from such social synchronization and the underlying evolutionary and ecological drivers that shape them remain poorly understood5–7,9. Here, we address this in the context of biparental care, a particularly sensitive phase of social synchronization12 where pair members potentially compromise their individual rhythms. Using data from 729 nests of 91 populations of 32 biparentally-incubating shorebird species, where parents synchronize to achieve continuous coverage of developing eggs, we report remarkable within– and between-species diversity in incubation rhythms. Between species, the median length of one parent’s incubation bout varied from 1 – 19 hours, while period length–the time in which a parent’s probability to incubate cycles once between its highest and lowest value – varied from 6 – 43 hours. The length of incubation bouts was unrelated to variables reflecting energetic demands, but species relying on crypsis (the ability to avoid detection by other animals) had longer incubation bouts than those that are readily visible or actively protect their nest against predators. Rhythms entrainable to the 24-h light-dark cycle were less prevalent at high latitudes and absent in 18 species. Our results indicate that even under similar environmental conditions and despite 24-h environmental cues, social synchronization can generate far more diverse behavioural rhythms than expected from studies of individuals in captivity5–7,9. The risk of predation, not the risk of starvation, may be a key factor underlying the diversity in these rhythms.

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Unexpected diversity in socially synchronized rhythms of shorebirds
Martin Bulla, Mihai Valcu, Adriaan M. Dokter, Alexei G. Dondua, András Kosztolányi, Anne Rutten, Barbara Helm, Brett K. Sandercock, Bruce Casler, Bruno J. Ens, Caleb S. Spiegel, Chris J. Hassell, Clemens Küpper, Clive Minton, Daniel Burgas, David B. Lank, David C. Payer, Egor Y. Loktinov, Erica Nol, Eunbi Kwon, Fletcher Smith, H. River Gates, Hana Vitnerová, Hanna Prüter, James A. Johnson, James J. H. St Clair, Jean-François Lamarre, Jennie Rausch, Jeroen Reneerkens, Jesse R. Conklin, Joana Burger, Joe Liebezeit, Joël Bêty, Jonathan T. Coleman, Jordi Figuerola, Jos C. E. W. Hooijmeijer, José A. Alves, Joseph A. M. Smith, Karel Weidinger, Kari Koivula, Ken Gosbell, Klaus-Michael Exo, Larry Niles, Laura Koloski, Laura McKinnon, Libor Praus, Marcel Klaassen, Marie-Andrée Giroux, Martin Sládeček, Megan L. Boldenow, Michael I. Goldstein, Miroslav šálek, Nathan Senner, Nelli Rönkä, Nicolas Lecomte, Olivier Gilg, Orsolya Vincze, Oscar W. Johnson, Paul A. Smith, Paul F. Woodard, Pavel S. Tomkovich, Phil F. Battley, Rebecca Bentzen, Richard B. Lanctot, Ron Porter, Sarah T. Saalfeld, Scott Freeman, Stephen C. Brown, Stephen Yezerinac, Tamás Székely, Tomás Montalvo, Theunis Piersma, Vanessa Loverti, Veli-Matti Pakanen, Wim Tijsen, Bart Kempenaers
bioRxiv 084806; doi: https://doi.org/10.1101/084806
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Unexpected diversity in socially synchronized rhythms of shorebirds
Martin Bulla, Mihai Valcu, Adriaan M. Dokter, Alexei G. Dondua, András Kosztolányi, Anne Rutten, Barbara Helm, Brett K. Sandercock, Bruce Casler, Bruno J. Ens, Caleb S. Spiegel, Chris J. Hassell, Clemens Küpper, Clive Minton, Daniel Burgas, David B. Lank, David C. Payer, Egor Y. Loktinov, Erica Nol, Eunbi Kwon, Fletcher Smith, H. River Gates, Hana Vitnerová, Hanna Prüter, James A. Johnson, James J. H. St Clair, Jean-François Lamarre, Jennie Rausch, Jeroen Reneerkens, Jesse R. Conklin, Joana Burger, Joe Liebezeit, Joël Bêty, Jonathan T. Coleman, Jordi Figuerola, Jos C. E. W. Hooijmeijer, José A. Alves, Joseph A. M. Smith, Karel Weidinger, Kari Koivula, Ken Gosbell, Klaus-Michael Exo, Larry Niles, Laura Koloski, Laura McKinnon, Libor Praus, Marcel Klaassen, Marie-Andrée Giroux, Martin Sládeček, Megan L. Boldenow, Michael I. Goldstein, Miroslav šálek, Nathan Senner, Nelli Rönkä, Nicolas Lecomte, Olivier Gilg, Orsolya Vincze, Oscar W. Johnson, Paul A. Smith, Paul F. Woodard, Pavel S. Tomkovich, Phil F. Battley, Rebecca Bentzen, Richard B. Lanctot, Ron Porter, Sarah T. Saalfeld, Scott Freeman, Stephen C. Brown, Stephen Yezerinac, Tamás Székely, Tomás Montalvo, Theunis Piersma, Vanessa Loverti, Veli-Matti Pakanen, Wim Tijsen, Bart Kempenaers
bioRxiv 084806; doi: https://doi.org/10.1101/084806

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