Letter | Published:

Unexpected diversity in socially synchronized rhythms of shorebirds

Nature volume 540, pages 109113 (01 December 2016) | Download Citation

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.

Access optionsAccess options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

References

  1. 1.

    , & Chronobiology: Biological Timekeeping (Sinauer Associates, 2004)

  2. 2.

    & Time zones: a comparative genetics of circadian clocks. Nat. Rev. Genet. 2, 702–715 (2001)

  3. 3.

    & Heritable circadian period length in a wild bird population. Proc. R. Soc. B 277, 3335–3342 (2010)

  4. 4.

    , , , & Heritability of diurnal type: a nationwide study of 8753 adult twin pairs. J. Sleep Res. 16, 156–162 (2007)

  5. 5.

    , & Animal clocks: when science meets nature. Proc. R. Soc. B 280, 20131354 (2013)

  6. 6.

    , , & Socially synchronized circadian oscillators. Proc. R. Soc. B 280, 20130035 (2013)

  7. 7.

    , & In search of a temporal niche: social interactions. Prog. Brain Res . 199, 267–280 (2012)

  8. 8.

    & Social influences on mammalian circadian rhythms: animal and human studies. Biol. Rev. Camb. Philos. Soc. 79, 533–556 (2004)

  9. 9.

    & Birds of a feather clock together–sometimes: social synchronization of circadian rhythms. Curr. Opin. Neurobiol. 13, 765–769 (2003)

  10. 10.

    Locomotor activity and non-photic influences on circadian clocks. Biol. Rev. Camb. Philos. Soc. 71, 343–372 (1996)

  11. 11.

    & Social influences on biological rhythms. Behaviour 72, 171–198 (1980)

  12. 12.

    & Ecology, sexual selection, and the evolution of mating systems. Science 197, 215–223 (1977)

  13. 13.

    Avian Incubation: Behaviour, Environment and Evolution (Oxford Univ. Press, 2002)

  14. 14.

    & Evolutionary transitions in parental care in shorebirds. Proc. R. Soc. B 262, 57–64 (1995)

  15. 15.

    , & Handbook of the Birds of the World. Vol. 3. Hoatzing to Auks . (Lynx Edicions, 1996)

  16. 16.

    et al. Supporting Information for ‘Unexpected diversity in socially synchronized rhythms of shorebirds’. Open Science Framework (2016)

  17. 17.

    in Avian Energetics and Nutritional Ecology (ed. ) Ch. 5, 375–416 (Chapman & Hall, 1996)

  18. 18.

    , , , & Biparental incubation-scheduling: no experimental evidence for major energetic constraints. Behav. Ecol. 26, 30–37 (2015)

  19. 19.

    , & Nest predation increases with parental activity: separating nest site and parental activity effects. Proc. R. Soc.B 267, 2287–2293 (2000)

  20. 20.

    , , , & Shorebird incubation behaviour and its influence on the risk of nest predation. Anim. Behav. 84, 835–842 (2012)

  21. 21.

    et al. Lower predation risk for migratory birds at high latitudes. Science 327, 326–327 (2010)

  22. 22.

    , , , & Latitudinal clines: an evolutionary view on biological rhythms. Proc. R. Soc. B 280, 20130433 (2013)

  23. 23.

    et al. Circadian organization in reindeer. Nature 438, 1095–1096 (2005)

  24. 24.

    et al. When the sun never sets: diverse activity rhythms under continuous daylight in free-living arctic-breeding birds. Proc. R. Soc. B 280, 20131016 (2013)

  25. 25.

    et al. Adaptive sleep loss in polygynous pectoral sandpipers. Science 337, 1654–1658 (2012)

  26. 26.

    & The rhythm of rest and excess. Nat. Rev. Neurosci. 6, 407–414 (2005)

  27. 27.

    & Reproductive mechanisms: interaction of circadian and interval timing. Ann. NY Acad. Sci . 423, 488–514 (1984)

  28. 28.

    , & Social synchronization of circadian rhythmicity in female mice depends on the number of cohabiting animals. Biol. Lett. 11, 20150204 (2015)

  29. 29.

    Two new graphical methods for mapping trait evolution on phylogenies. Methods Ecol. Evol . 4, 754–759 (2013)

  30. 30.

    Phylogenies and the comparative method. Am. Nat. 125, 1–15 (1985)

  31. 31.

    , , & Biparental incubation patterns in a high-Arctic breeding shorebird: how do pairs divide their duties? Behav. Ecol. 25, 152–164 (2014)

  32. 32.

    , , , & Do uniparental sanderlings Calidris alba increase egg heat input to compensate for low nest attentiveness? PLoS One 6, e16834 (2011)

  33. 33.

    & Using a transponder system to monitor incubation routines of Snowy Plovers. J. Field Ornithol. 73, 199–205 (2002)

  34. 34.

    & Attachment of geolocators to bar-tailed godwits: a tibia-mounted method with no survival effects or loss of units. Wader Study Group Bull . 117, 56–58 (2010)

  35. 35.

    , , & Using geolocator data to reveal incubation periods and breeding biology in Red Knots Calidris canutus rufa. Wader Study Group Bull . 119, 26–36 (2012)

  36. 36.

    , , & A flexible GPS tracking system for studying bird behaviour at multiple scales. J. Ornithol. 154, 571–580 (2012)

  37. 37.

    R-SCRIPT and EXAMPLE DATA to extract incubation from temperature measurements. Version 1. figshare (2014)

  38. 38.

    R-SCRIPT and EXAMPLE DATA to extract incubation bouts from continuous RFID and video data. Version 1. figshare (2015)

  39. 39.

    Example of how to manually extract incubation bouts from interactive plots of raw data—R-CODE and DATA. Version 1. figshare (2016)

  40. 40.

    Procedure for manual extraction of incubation bouts from plots of raw data.pdf. Version 1. figshare (2016)

  41. 41.

    ggplot2: Elegant Graphics for Data Analysis (Springer 2009)

  42. 42.

    & latticeExtra: Extra Graphical Utilities Based on Lattice. R package version 0.6-24 (2012)

  43. 43.

    Lattice: Multivariate Data Visualization with R (Springer, 2008)

  44. 44.

    Geolocator-ArcticWader-BreedingSiteEstimation. Version 2015-08-05. GitHub repository (2015)

  45. 45.

    & GeoLight—processing and analysing light-based geolocator data in R. Methods Ecol. Evol . 3, 1055–1059 (2012)

  46. 46.

    et al. Geolocation by light: accuracy and precision affected by environmental factors. Methods Ecol. Evol . 3, 603–612 (2012)

  47. 47.

    , , & Breeding latitude drives individual schedules in a trans-hemispheric migrant bird. Nat. Commun. 1, 67 (2010)

  48. 48.

    The Birds of North America (Cornell Laboratory of Ornithology, 2005)

  49. 49.

    , & Atlas of Breeding Waders in the Russian Arctic (UF Ofsetnaya Pecha, 2012)

  50. 50.

    Shorebirds of the Northern Hemisphere (Christopher Helm, 2009)

  51. 51.

    Birds of East Asia: Eastern China, Taiwan, Korea, Japan, and Eastern Russia (Christopher Helm, 2009)

  52. 52.

    et al. Sexual selection explains Rensch’s rule of allometry for sexual size dimorphism. Proc. R. Soc.B 274, 2971–2979 (2007)

  53. 53.

    et al. Supplementary Data 3—Study sites: location, population wing length, monitoring method, tide. Version 11. figshare (2016)

  54. 54.

    Handbook of the Birds of Europe, the Middle East, and North Africa: The Birds of the Western Palearctic Volume III: Waders to Gulls (Oxford Univ. Press, 1990)

  55. 55.

    , & Phylogenetic analysis and comparative data: a test and review of evidence. Am. Nat. 160, 712–726 (2002)

  56. 56.

    Inferring evolutionary processes from phylogenies. Zool. Scr. 26, 331–348 (1997)

  57. 57.

    & Phylogenies and the comparative method: a general approach to incorporating phylogenetic information into the analysis of interspecific data. Am. Nat. 149, 646–667 (1997)

  58. 58.

    Inferring the historical patterns of biological evolution. Nature 401, 877–884 (1999)

  59. 59.

    et al. A phylogenomic study of birds reveals their evolutionary history. Science 320, 1763–1768 (2008)

  60. 60.

    , , , & The global diversity of birds in space and time. Nature 491, 444–448 (2012)

  61. 61.

    et al. Kentish versus snowy plover: phenotypic and genetic analyses of Charadrius alexandrinus reveal divergence of Eurasian and American subspecies. Auk 126, 839–852 (2009)

  62. 62.

    MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J. Stat. Softw. 33, 1–22 (2010)

  63. 63.

    R-Core-Team. R: A Language and Environment for Statistical Computing. Version 3.1.1. R Foundation for Statistical Computing (2014)

  64. 64.

    Model Based Inference in the Life Sciences: A Primer on Evidence (Springer, 2008)

  65. 65.

    raster: Geographic data analysis and modeling. R package version 2.3-24. (2015)

  66. 66.

    & maptools: Tools for reading and handling spatial objects. R package version 0.8-30. (2014)

  67. 67.

    in Modern Phylogenetic Comparative Methods and Their Application in Evolutionary Biology (ed. ) Ch. 4, 77–103 (Springer, 2014)

  68. 68.

    et al. Tracking Pacific golden-plovers Pluvialis fulva: transoceanic migrations between non-breeding grounds in Kwajalein, Japan and Hawaii and breeding grounds in Alaska and Chukotka. Wader Study 122, 13–20 (2015)

  69. 69.

    , & Negotiation between parents over care: reversible compensation during incubation. Behav. Ecol. 20, 446–452 (2009)

  70. 70.

    , , & Female-biased incubation and strong diel sex-roles in the two-banded plover Charadrius falklandicus. J. Ornithol. 151, 811–816 (2010)

  71. 71.

    , , & Factors affecting incubation patterns and sex roles of black oystercatchers in Alaska. Condor 114, 123–134 (2012)

  72. 72.

    & Predators and nest success of sky larks Alauda arvensis in large arable fields in the Czech Republic. Bird Study 57, 525–530 (2010)

  73. 73.

    et al. caper: Comparative Analyses of Phylogenetics and Evolution in R. R package version 0.5.2. (2013)

Download references

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

Authors

  1. Search for Martin Bulla in:

  2. Search for Mihai Valcu in:

  3. Search for Adriaan M. Dokter in:

  4. Search for Alexei G. Dondua in:

  5. Search for András Kosztolányi in:

  6. Search for Anne L. Rutten in:

  7. Search for Barbara Helm in:

  8. Search for Brett K. Sandercock in:

  9. Search for Bruce Casler in:

  10. Search for Bruno J. Ens in:

  11. Search for Caleb S. Spiegel in:

  12. Search for Chris J. Hassell in:

  13. Search for Clemens Küpper in:

  14. Search for Clive Minton in:

  15. Search for Daniel Burgas in:

  16. Search for David B. Lank in:

  17. Search for David C. Payer in:

  18. Search for Egor Y. Loktionov in:

  19. Search for Erica Nol in:

  20. Search for Eunbi Kwon in:

  21. Search for Fletcher Smith in:

  22. Search for H. River Gates in:

  23. Search for Hana Vitnerová in:

  24. Search for Hanna Prüter in:

  25. Search for James A. Johnson in:

  26. Search for James J. H. St Clair in:

  27. Search for Jean-François Lamarre in:

  28. Search for Jennie Rausch in:

  29. Search for Jeroen Reneerkens in:

  30. Search for Jesse R. Conklin in:

  31. Search for Joanna Burger in:

  32. Search for Joe Liebezeit in:

  33. Search for Joël Bêty in:

  34. Search for Jonathan T. Coleman in:

  35. Search for Jordi Figuerola in:

  36. Search for Jos C. E. W. Hooijmeijer in:

  37. Search for José A. Alves in:

  38. Search for Joseph A. M. Smith in:

  39. Search for Karel Weidinger in:

  40. Search for Kari Koivula in:

  41. Search for Ken Gosbell in:

  42. Search for Klaus-Michael Exo in:

  43. Search for Larry Niles in:

  44. Search for Laura Koloski in:

  45. Search for Laura McKinnon in:

  46. Search for Libor Praus in:

  47. Search for Marcel Klaassen in:

  48. Search for Marie-Andrée Giroux in:

  49. Search for Martin Sládeček in:

  50. Search for Megan L. Boldenow in:

  51. Search for Michael I. Goldstein in:

  52. Search for Miroslav Šálek in:

  53. Search for Nathan Senner in:

  54. Search for Nelli Rönkä in:

  55. Search for Nicolas Lecomte in:

  56. Search for Olivier Gilg in:

  57. Search for Orsolya Vincze in:

  58. Search for Oscar W. Johnson in:

  59. Search for Paul A. Smith in:

  60. Search for Paul F. Woodard in:

  61. Search for Pavel S. Tomkovich in:

  62. Search for Phil F. Battley in:

  63. Search for Rebecca Bentzen in:

  64. Search for Richard B. Lanctot in:

  65. Search for Ron Porter in:

  66. Search for Sarah T. Saalfeld in:

  67. Search for Scott Freeman in:

  68. Search for Stephen C. Brown in:

  69. Search for Stephen Yezerinac in:

  70. Search for Tamás Székely in:

  71. Search for Tomás Montalvo in:

  72. Search for Theunis Piersma in:

  73. Search for Vanessa Loverti in:

  74. Search for Veli-Matti Pakanen in:

  75. Search for Wim Tijsen in:

  76. Search for Bart Kempenaers in:

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

About this article

Publication history

Received

Accepted

Published

DOI

https://doi.org/10.1038/nature20563

Further reading

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.