Unexpected diversity in socially synchronized rhythms of shorebirds.

Nature. 2016 Dec 1;540(7631):109-113. doi: 10.1038/nature20563. Epub 2016 Nov 23. Bulla M1, Valcu M1, Dokter AM2, Dondua AG3, Kosztolányi A4,5, Rutten AL1,6, Helm B7, Sandercock BK8, Casler B, Ens BJ9, Spiegel CS10, Hassell CJ11, Küpper C12, Minton C13, Burgas D14,15, Lank DB16, Payer DC17, Loktionov EY18, Nol E19, Kwon E20, Smith F21, Gates HR22,23,24, Vitnerová H25, Prüter H26, Johnson JA23, St Clair JJ27,28, Lamarre JF29, Rausch J30, Reneerkens J31, Conklin JR31, Burger J32, Liebezeit J33, Bêty J29, Coleman JT34, Figuerola J35, Hooijmeijer JC31, Alves JA36,37, Smith JA38, Weidinger K39, Koivula K40, Gosbell K41, Exo KM42, Niles L43, Koloski L44, McKinnon L45, Praus L39, Klaassen M46, Giroux MA47,48, Sládeček M49, Boldenow ML50, Goldstein MI51, Šálek M49, Senner N31,52, Rönkä N40, Lecomte N48, Gilg O53,54, Vincze O5,55, Johnson OW56, Smith PA57, Woodard PF30, Tomkovich PS58, Battley PF59, Bentzen R60, Lanctot RB23, Porter R61, Saalfeld ST23, Freeman S62, Brown SC24, Yezerinac S63, Székely T64, Montalvo T65, Piersma T31,66, Loverti V67, Pakanen VM40, Tijsen W68, Kempenaers B1. Author information 1 Department of Behavioural Ecology and Evolutionary Genetics, Max Planck Institute for Ornithology, Eberhard Gwinner Str, Seewiesen 82319, Germany. 2 Computational Geo-Ecology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Science Park 904, Amsterdam 1098 XH, The Netherlands. 3 Gatchinskaya, apartment 27, Saint Petersburg 197198, Russia. 4 Department of Ecology, University of Veterinary Medicine Budapest, Rottenbiller u. 50, Budapest H-1077, Hungary. 5 MTA-DE 'Lendület' Behavioural Ecology Research Group, Department of Evolutionary Zoology, University of Debrecen, Egyetem tér 1, Debrecen H-4032, Hungary. 6 Apiloa GmbH, Starnberg 82319, Germany. 7 Institute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, Graham Kerr Building, Glasgow G12 8QQ, UK. 8 Division of Biology, Kansas State University, 116 Ackert Hall, Manhattan, Kansas 66506-4901, USA. 9 Coastal Ecology Team, Sovon Dutch Centre for Field Ornithology, PO Box 59, Den Burg 1790 AB, Texel, The Netherlands. 10 Division of Migratory Birds, Northeast Region, US Fish and Wildlife Service, 300 Westgate Center Dr, Hadley, Massachusetts 01035, USA. 11 Global Flyway Network, PO Box 3089, Broome, Western Australia 6725, Australia. 12 Institute of Zoology, University of Graz, Universitätsplatz 2, 8010 Graz, Austria. 13 Victorian Wader Study group, 165 Dalgetty Road, Beaumaris, Melbourne, Victoria 3193, Australia. 14 Department of Forest Sciences, University of Helsinki, PO Box 27, Helsinki FI-00014, Finland. 15 Department of Biological and Environmental Sciences, University of Jyväskylä, PO Box 35, Jyväskylä FI-40014, Finland. 16 Department of Biological Sciences, Simon Fraser University, 8888 University Drive, Burnaby, British Columbia V5A 1S6, Canada. 17 Alaska Region, US National Park Service, 240 W 5th Ave, Anchorage, Alaska 99501, USA. 18 State Lab for Photon Energetics, Bauman Moscow State Technical University, 2nd Baumanskaya St, 5-1, Moscow 105005, Russia. 19 Biology Department, Trent University, 2140 East Bank Drive, Peterborough, Ontario K9L 0G2, Canada. 20 Department of Fish and Wildlife Conservation, Virginia Polytechnic Institute and State University, 310 West Campus Drive, Blacksburg, Virginia 24061, USA. 21 Center for Conservation Biology, College of William &Mary and Virginia Commonwealth University, PO Box 8795, Williamsburg, Virginia 23187, USA. 22 Pacifica Ecological Services, 17520 Snow Crest Lane, Anchorage, Alaska, 99516, USA. 23 Migratory Bird Management, US Fish and Wildlife Service, 1011 East Tudor Road, Anchorage, Alaska 99503, USA. 24 Shorebird Recovery Program, Manomet, PO Box 545, Saxtons River, Vermont 05154, USA. 25 Faculty of Science, Charles University in Prague, Albertov 6, Praha 128 43, Czech Republic. 26 Department of Wildlife Diseases, Leibniz Institute for Zoo- and Wildlife Research, Alfred-Kowalke-Straße 17, Berlin 10315, Germany. 27 Biodiversity Lab, Department of Biology and Biochemistry, University of Bath, Claverton Down, Bath BA1 7AY, UK. 28 Centre for Evolutionary Biology, School of Biology, University of Western Australia, Stirling Highway, Crawley, Western Australia 6009, Australia. 29 Département 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. 30 Canadian Wildlife Service, Environment and Climate Change Canada, PO Box 2310, 5019-52nd Street, 4th Floor, Yellowknife, Northwest Territories X1A 2P7, Canada. 31 Conservation Ecology Group, Groningen Institute for Evolutionary Life Sciences, University of Groningen, Nijenborgh 7, Groningen 9747 AG, The Netherlands. 32 Division of Life Sciences, Rutgers University, 604-Allison Road, Piscataway, New Jersey 08854-8082, USA. 33 Audubon Society of Portland, 5151 NW Cornell Road, Portland, Oregon 97210, USA. 34 Queensland Wader Study Group, 22 Parker Street, Brisbane, Queensland 4128, Australia. 35 Department of Wetland Ecology, Doñana Biological Station (CSIC), Av. Américo Vespucio, s/n, Seville 41092, Spain. 36 Centre for Environmental and Marine Studies (CESAM), Department of Biology, University of Aveiro, Campus de Santiago, Aveiro 3810-193, Portugal. 37 South Iceland Research Centre, University of Iceland, Fjolheimar, Selfoss 800, Iceland. 38 LJ Niles Associates, PO Box 784, Cape May, New Jersey 08204, USA. 39 Department of Zoology and Laboratory of Ornithology, Palacký University, 17. Listopadu 50, Olomouc 771 46, Czech Republic. 40 Department of Ecology, University of Oulu, PO Box 3000, Oulu 90014, Finland. 41 Australasian Wader Studies Group, 1/19 Baldwin Road, Blackburn, Melbourne, Victoria 3130, Australia. 42 Institute of Avian Research, Vogelwarte Helgoland, An der Vogelwarte 21, Wilhelmshaven D-26386, Germany. 43 LJ Niles Associates, 109 Market Lane, Greenwich, Connecticut 08323, USA. 44 Environmental and Life Sciences, Trent University, 1600 West Bank Dr, Peterborough, Ontario K0L 0G2, Canada. 45 Bilingual Biology Program, York University Glendon Campus, 2275 Bayview Avenue, Toronto, Ontario M4N 3M6, Canada. 46 Centre for Integrative Ecology, Deakin University, 75 Pigdons Road, Waurn Ponds, Geelong, Victoria 3216, Australia. 47 Canada Research in Northern Biodiversity and Centre d'Études Nordiques, Université du Québec à Rimouski, 300, Allée des Ursulines, Rimouski, Quebec G5L 3A8, Canada. 48 Canada Research in Polar and Boreal Ecology and Centre d'Études Nordiques, Université de Moncton, 18 avenue Antonine-Maillet, Moncton, New Brunswick E4K 1A6, Canada. 49 Faculty of Environmental Sciences, Czech University of Life Sciences Prague, Kamýcká 1176, Suchdol, Prague 16521, Czech Republic. 50 Department of Biology and Wildlife, University of Alaska Fairbanks, PO Box 756100, Fairbanks, Alaska 99775-6100, USA. 51 Alaska Coastal Rainforest Center, University of Alaska Southeast, 11120 Glacier Hwy, Juneau, Alaska 99801, USA. 52 Cornell Lab of Ornithology, 159 Sapsucker Woods Road, Ithaca 14850, USA. 53 Equipe Ecologie Evolution, UMR 6282 Biogéosciences, Université de Bourgogne Franche Comté, 6 Bd Gabriel, Dijon 21000, France. 54 Groupe de Recherche en Ecologie Arctique, 16 Rue de Vernot, Francheville 21440, France. 55 Evolutionary Ecology Group, Hungarian Department of Biology and Ecology, Babeş-Bolyai University, Clinicilor 5-7, Cluj-Napoca RO-400006, Romania. 56 Department of Ecology, Montana State University, Bozeman, Montana 59717, USA. 57 Wildlife Research Division, Environment and Climate Change Canada, 1125 Colonel By Dr, Ottawa, Ontario K1A 0H3, Canada. 58 Zoological Museum, Lomonosov Moscow State University, Bolshaya Nikitskaya St, 6, Moscow 125009, Russia. 59 Institute of Agriculture &Environment, Massey University, Private Bag 11 222, Palmerston North 4442, New Zealand. 60 Arctic Beringia Program, Wildlife Conservation Society, 925 Schloesser Dr, Fairbanks, Alaska 99709, USA. 61 Delaware Bay Shorebird Project, Ambler, Pennsylvania 19002, USA. 62 Arctic National Wildlife Refuge, US Fish and Wildlife Service, 101 12th Ave, Fairbanks, Alaska 99701, USA. 63 Fieldday Consulting, Surrey, British Columbia V4N 6M5, Canada. 64 Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, Claverton Down, Bath BA2 7AY, UK. 65 Servei de Vigilància i Control de Plagues Urbanes, Agència de Salut Pública de Barcelona, Av. Príncep d'Astúries 63, Barcelona 8012, Spain. 66 NIOZ Royal Netherlands Institute for Sea Research, Department of Coastal Systems and Utrecht University, PO Box 59, Den Burg 1790 AB, Texel, The Netherlands. 67 Migratory Bird and Habitat Program, US Fish and Wildlife Service, 911 NE 11th Avenue, Portland, Oregon 97232, USA. 68 Poelweg 12, Westerland 1778 KB, The Netherlands. Abstract The behavioural rhythms of organisms are thought to be under strong selection, influenced by the rhythmicity of the environment. Such behavioural rhythms are well studied in isolated individuals under laboratory conditions, but free-living individuals have to temporally synchronize their activities with those of others, including potential mates, competitors, prey and predators. Individuals can temporally segregate their daily activities (for example, prey avoiding predators, subordinates avoiding dominants) or synchronize their activities (for example, group foraging, communal defence, pairs reproducing or caring for offspring). The behavioural rhythms that emerge from such social synchronization and the underlying evolutionary and ecological drivers that shape them remain poorly understood. Here we investigate these rhythms in the context of biparental care, a particularly sensitive phase of social synchronization 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 h, whereas period length-the time in which a parent's probability to incubate cycles once between its highest and lowest value-varied from 6-43 h. 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 who 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 captivity. The risk of predation, not the risk of starvation, may be a key factor underlying the diversity in these rhythms. Comment in Biological rhythms: Wild times. [Nature. 2016] PMID: 27880762 DOI: 10.1038/nature20563 [Indexed for MEDLINE]