Letter | Published:

Unexpected diversity in socially synchronized rhythms of shorebirds

Nature 540, 109–113 (01 December 2016) | Download Citation

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Abstract

The behavioural rhythms of organisms are thought to be under strong selection, influenced by the rhythmicity of the environment1,2,3,4. 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 predators6,7,8,9,10. 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)6,7,8,9,11. The behavioural rhythms that emerge from such social synchronization and the underlying evolutionary and ecological drivers that shape them remain poorly understood5,6,7,9. Here we investigate these rhythms 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 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 captivity5,6,7,9. The risk of predation, not the risk of starvation, may be a key factor underlying the diversity in these rhythms.

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Acknowledgements

We thank all that made the data collection possible. We are grateful to W. Schwartz, E. Schlicht, W. Forstmeier, M. Baldwin, H. Fried Petersen, D. Starr-Glass and B. Bulla for comments on the manuscript and to F. Korner-Nievergelt, J. D. Hadfield, L. Z. Garamszegi, S. Nakagawa, T. Roth, N. Dochtermann, Y. Araya, E. Miller and H. Schielzeth for advice on data analysis. Data collection was supported by various institutions and people listed in supplementary data 1 at https://osf.io/sq8gk (ref. 16). The study was supported by the Max Planck Society (to B.K.). M.B. is a PhD student in the International Max Planck Research School for Organismal Biology.

Author information

Affiliations

  1. Department of Behavioural Ecology and Evolutionary Genetics, Max Planck Institute for Ornithology, Eberhard Gwinner Str, Seewiesen 82319, Germany

    • Martin Bulla
    • , Mihai Valcu
    • , Anne L. Rutten
    •  & Bart Kempenaers

  2. Computational Geo-Ecology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Science Park 904, Amsterdam 1098 XH, The Netherlands

    • Adriaan M. Dokter

  3. Gatchinskaya, apartment 27, Saint Petersburg 197198, Russia

    • Alexei G. Dondua

  4. Department of Ecology, University of Veterinary Medicine Budapest, Rottenbiller u. 50, Budapest H-1077, Hungary

    • András Kosztolányi

  5. MTA-DE ‘Lendület’ Behavioural Ecology Research Group, Department of Evolutionary Zoology, University of Debrecen, Egyetem tér 1, Debrecen H-4032, Hungary

    • András Kosztolányi
    •  & Orsolya Vincze

  6. Apiloa GmbH, Starnberg 82319, Germany

    • Anne L. Rutten

  7. Institute of Biodiversity, Animal Health and Comparative Medicine, University of Glasgow, Graham Kerr Building, Glasgow G12 8QQ, UK

    • Barbara Helm

  8. Division of Biology, Kansas State University, 116 Ackert Hall, Manhattan, Kansas 66506-4901, USA

    • Brett K. Sandercock

  9. PO Box 1094, Fallon, Nevada 89407, USA

    • Bruce Casler

  10. Coastal Ecology Team, Sovon Dutch Centre for Field Ornithology, PO Box 59, Den Burg 1790 AB, Texel, The Netherlands

    • Bruno J. Ens

  11. Division of Migratory Birds, Northeast Region, US Fish and Wildlife Service, 300 Westgate Center Dr, Hadley, Massachusetts 01035, USA

    • Caleb S. Spiegel

  12. Global Flyway Network, PO Box 3089, Broome, Western Australia 6725, Australia

    • Chris J. Hassell

  13. Institute of Zoology, University of Graz, Universitätsplatz 2, 8010 Graz, Austria

    • Clemens Küpper

  14. Victorian Wader Study group, 165 Dalgetty Road, Beaumaris, Melbourne, Victoria 3193, Australia

    • Clive Minton

  15. Department of Forest Sciences, University of Helsinki, PO Box 27, Helsinki FI-00014, Finland

    • Daniel Burgas

  16. Department of Biological and Environmental Sciences, University of Jyväskylä, PO Box 35, Jyväskylä FI-40014, Finland

    • Daniel Burgas

  17. Department of Biological Sciences, Simon Fraser University, 8888 University Drive, Burnaby, British Columbia V5A 1S6, Canada

    • David B. Lank

  18. Alaska Region, US National Park Service, 240 W 5th Ave, Anchorage, Alaska 99501, USA

    • David C. Payer

  19. State Lab for Photon Energetics, Bauman Moscow State Technical University, 2nd Baumanskaya St, 5-1, Moscow 105005, Russia

    • Egor Y. Loktionov

  20. Biology Department, Trent University, 2140 East Bank Drive, Peterborough, Ontario K9L 0G2, Canada

    • Erica Nol

  21. Department of Fish and Wildlife Conservation, Virginia Polytechnic Institute and State University, 310 West Campus Drive, Blacksburg, Virginia 24061, USA

    • Eunbi Kwon

  22. Center for Conservation Biology, College of William & Mary and Virginia Commonwealth University, PO Box 8795, Williamsburg, Virginia 23187, USA

    • Fletcher Smith

  23. Pacifica Ecological Services, 17520 Snow Crest Lane, Anchorage, Alaska, 99516, USA

    • H. River Gates

  24. Migratory Bird Management, US Fish and Wildlife Service, 1011 East Tudor Road, Anchorage, Alaska 99503, USA

    • H. River Gates
    • , James A. Johnson
    • , Richard B. Lanctot
    •  & Sarah T. Saalfeld

  25. Shorebird Recovery Program, Manomet, PO Box 545, Saxtons River, Vermont 05154, USA

    • H. River Gates
    •  & Stephen C. Brown

  26. Faculty of Science, Charles University in Prague, Albertov 6, Praha 128 43, Czech Republic

    • Hana Vitnerová

  27. Department of Wildlife Diseases, Leibniz Institute for Zoo- and Wildlife Research, Alfred-Kowalke-Straße 17, Berlin 10315, Germany

    • Hanna Prüter

  28. Biodiversity Lab, Department of Biology and Biochemistry, University of Bath, Claverton Down, Bath BA1 7AY, UK

    • James J. H. St Clair

  29. Centre for Evolutionary Biology, School of Biology, University of Western Australia, Stirling Highway, Crawley, Western Australia 6009, Australia

    • James J. H. St Clair

  30. 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

    • Jean-François Lamarre
    •  & Joël Bêty

  31. Canadian Wildlife Service, Environment and Climate Change Canada, PO Box 2310, 5019—52nd Street, 4th Floor, Yellowknife, Northwest Territories X1A 2P7, Canada

    • Jennie Rausch
    •  & Paul F. Woodard

  32. Conservation Ecology Group, Groningen Institute for Evolutionary Life Sciences, University of Groningen, Nijenborgh 7, Groningen 9747 AG, The Netherlands

    • Jeroen Reneerkens
    • , Jesse R. Conklin
    • , Jos C. E. W. Hooijmeijer
    • , Nathan Senner
    •  & Theunis Piersma

  33. Division of Life Sciences, Rutgers University, 604-Allison Road, Piscataway, New Jersey 08854-8082, USA

    • Joanna Burger

  34. Audubon Society of Portland, 5151 NW Cornell Road, Portland, Oregon 97210, USA

    • Joe Liebezeit

  35. Queensland Wader Study Group, 22 Parker Street, Brisbane, Queensland 4128, Australia

    • Jonathan T. Coleman

  36. Department of Wetland Ecology, Doñana Biological Station (CSIC), Av. Américo Vespucio, s/n, Seville 41092, Spain

    • Jordi Figuerola

  37. Centre for Environmental and Marine Studies (CESAM), Department of Biology, University of Aveiro, Campus de Santiago, Aveiro 3810-193, Portugal

    • José A. Alves

  38. South Iceland Research Centre, University of Iceland, Fjolheimar, Selfoss 800, Iceland

    • José A. Alves

  39. LJ Niles Associates, PO Box 784, Cape May, New Jersey 08204, USA

    • Joseph A. M. Smith

  40. Department of Zoology and Laboratory of Ornithology, Palacký University, 17. Listopadu 50, Olomouc 771 46, Czech Republic

    • Karel Weidinger
    •  & Libor Praus

  41. Department of Ecology, University of Oulu, PO Box 3000, Oulu 90014, Finland

    • Kari Koivula
    • , Nelli Rönkä
    •  & Veli-Matti Pakanen

  42. Australasian Wader Studies Group, 1/19 Baldwin Road, Blackburn, Melbourne, Victoria 3130, Australia

    • Ken Gosbell

  43. Institute of Avian Research, Vogelwarte Helgoland, An der Vogelwarte 21, Wilhelmshaven D-26386, Germany

    • Klaus-Michael Exo

  44. LJ Niles Associates, 109 Market Lane, Greenwich, Connecticut 08323, USA

    • Larry Niles

  45. Environmental and Life Sciences, Trent University, 1600 West Bank Dr, Peterborough, Ontario K0L 0G2, Canada

    • Laura Koloski

  46. Bilingual Biology Program, York University Glendon Campus, 2275 Bayview Avenue, Toronto, Ontario M4N 3M6, Canada

    • Laura McKinnon

  47. Centre for Integrative Ecology, Deakin University, 75 Pigdons Road, Waurn Ponds, Geelong, Victoria 3216, Australia

    • Marcel Klaassen

  48. Canada Research in Northern Biodiversity and Centre d'Études Nordiques, Université du Québec à Rimouski, 300, Allée des Ursulines, Rimouski, Quebec G5L 3A8, Canada

    • Marie-Andrée Giroux

  49. 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

    • Marie-Andrée Giroux
    •  & Nicolas Lecomte

  50. Faculty of Environmental Sciences, Czech University of Life Sciences Prague, Kamýcká 1176, Suchdol, Prague 16521, Czech Republic

    • Martin Sládeček
    •  & Miroslav Šálek

  51. Department of Biology and Wildlife, University of Alaska Fairbanks, PO Box 756100, Fairbanks, Alaska 99775-6100, USA

    • Megan L. Boldenow

  52. Alaska Coastal Rainforest Center, University of Alaska Southeast, 11120 Glacier Hwy, Juneau, Alaska 99801, USA

    • Michael I. Goldstein

  53. Cornell Lab of Ornithology, 159 Sapsucker Woods Road, Ithaca 14850, USA

    • Nathan Senner

  54. Equipe Ecologie Evolution, UMR 6282 Biogéosciences, Université de Bourgogne Franche Comté, 6 Bd Gabriel, Dijon 21000, France

    • Olivier Gilg

  55. Groupe de Recherche en Ecologie Arctique, 16 Rue de Vernot, Francheville 21440, France

    • Olivier Gilg

  56. Evolutionary Ecology Group, Hungarian Department of Biology and Ecology, Babeş-Bolyai University, Clinicilor 5-7, Cluj-Napoca RO-400006, Romania

    • Orsolya Vincze

  57. Department of Ecology, Montana State University, Bozeman, Montana 59717, USA

    • Oscar W. Johnson

  58. Wildlife Research Division, Environment and Climate Change Canada, 1125 Colonel By Dr, Ottawa, Ontario K1A 0H3, Canada

    • Paul A. Smith

  59. Zoological Museum, Lomonosov Moscow State University, Bolshaya Nikitskaya St, 6, Moscow 125009, Russia

    • Pavel S. Tomkovich

  60. Institute of Agriculture & Environment, Massey University, Private Bag 11 222, Palmerston North 4442, New Zealand

    • Phil F. Battley

  61. Arctic Beringia Program, Wildlife Conservation Society, 925 Schloesser Dr, Fairbanks, Alaska 99709, USA

    • Rebecca Bentzen

  62. Delaware Bay Shorebird Project, Ambler, Pennsylvania 19002, USA

    • Ron Porter

  63. Arctic National Wildlife Refuge, US Fish and Wildlife Service, 101 12th Ave, Fairbanks, Alaska 99701, USA

    • Scott Freeman

  64. Fieldday Consulting, Surrey, British Columbia V4N 6M5, Canada

    • Stephen Yezerinac

  65. Milner Centre for Evolution, Department of Biology and Biochemistry, University of Bath, Claverton Down, Bath BA2 7AY, UK

    • Tamás Székely

  66. Servei de Vigilància i Control de Plagues Urbanes, Agència de Salut Pública de Barcelona, Av. Príncep d’Astúries 63, Barcelona 8012, Spain

    • Tomás Montalvo

  67. NIOZ Royal Netherlands Institute for Sea Research, Department of Coastal Systems and Utrecht University, PO Box 59, Den Burg 1790 AB, Texel, The Netherlands

    • Theunis Piersma

  68. Migratory Bird and Habitat Program, US Fish and Wildlife Service, 911 NE 11th Avenue, Portland, Oregon 97232, USA

    • Vanessa Loverti

  69. Poelweg 12, Westerland 1778 KB, The Netherlands

    • Wim Tijsen

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Contributions

M.B. and B.K. conceived the study. All authors except B.H. collected the primary data (see https://osf.io/sq8gk, ref. 16). M.B. coordinated the study and managed the data. M.B. and M.V. developed the methods to extract incubation. M.B. extracted bout lengths and with help from A.R. and M.V. created actograms. M.B. analysed the data with help from M.V. M.B. prepared the supporting information. M.B. and B.K. wrote the paper with input from the other authors. Except for the first, second and last author, the authors are listed alphabetically by their first name.

Competing interests

The authors declare no competing financial interests.

Corresponding authors

Correspondence to Martin Bulla or Bart Kempenaers.

Reviewer Information Nature thanks P. Bartell, C. Buck and M. Visser for their contribution to the peer review of this work.

Extended data

Extended data figures

  1. 1.

    Extracting period length of incubation rhythms.

  2. 2.

    Extracting incubation bouts from light-logger data.

  3. 3.

    Relationship between bout and period length for 30 shorebird species.

  4. 4.

    Ecological correlates of latitude.

  5. 5.

    Between-species variation in parental crypsis during incubation.

  6. 6.

    Phylogenetic relationships for predictors.

Extended data tables

  1. 1.

    Incubation monitoring methods and systems

  2. 2.

    Effects of phylogeny and sampling on bout length and period length

  3. 3.

    Source of phylogenetic signal

  4. 4.

    Effect of latitude, body size, escape distance and life history on biparental incubation rhythms in shorebirds

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DOI

https://doi.org/10.1038/nature20563

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