Unexpected diversity in socially synchronized rhythms of shorebirds

Martin Bulla, Mihai Valcu, Adriaan M. Dokter, Alexei G. Dondua, András Kosztolányi, Anne L. 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. Loktionov, Erica Nol, Eunbi Kwon & 56 others 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, Joanna 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 Andreé Giroux, Martin Sládecek, 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

Research output: Contribution to journalArticle

46 Citations (Scopus)
41 Downloads (Pure)

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.

Original languageEnglish
Pages (from-to)109-113
Number of pages5
JournalNature
Volume540
Issue number7631
Early online date23 Nov 2016
DOIs
Publication statusPublished - 1 Dec 2016

Fingerprint

predators
nests
starvation
photoperiod
foraging
predation
species diversity
environmental factors
organisms
animals

Cite this

Bulla, M., Valcu, M., Dokter, A. M., Dondua, A. G., Kosztolányi, A., Rutten, A. L., ... Kempenaers, B. (2016). Unexpected diversity in socially synchronized rhythms of shorebirds. Nature, 540(7631), 109-113. https://doi.org/10.1038/nature20563

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

In: Nature, Vol. 540, No. 7631, 01.12.2016, p. 109-113.

Research output: Contribution to journalArticle

Bulla, M, Valcu, M, Dokter, AM, Dondua, AG, Kosztolányi, A, Rutten, AL, Helm, B, Sandercock, BK, Casler, B, Ens, BJ, Spiegel, CS, Hassell, CJ, Küpper, C, Minton, C, Burgas, D, Lank, DB, Payer, DC, Loktionov, EY, Nol, E, Kwon, E, Smith, F, Gates, HR, Vitnerová, H, Prüter, H, Johnson, JA, St Clair, JJH, Lamarre, JF, Rausch, J, Reneerkens, J, Conklin, JR, Burger, J, Liebezeit, J, Bêty, J, Coleman, JT, Figuerola, J, Hooijmeijer, JCEW, Alves, JA, Smith, JAM, Weidinger, K, Koivula, K, Gosbell, K, Exo, KM, Niles, L, Koloski, L, McKinnon, L, Praus, L, Klaassen, M, Giroux, MA, Sládecek, M, Boldenow, ML, Goldstein, MI, Šálek, M, Senner, N, Rönkä, N, Lecomte, N, Gilg, O, Vincze, O, Johnson, OW, Smith, PA, Woodard, PF, Tomkovich, PS, Battley, PF, Bentzen, R, Lanctot, RB, Porter, R, Saalfeld, ST, Freeman, S, Brown, SC, Yezerinac, S, Székely, T, Montalvo, T, Piersma, T, Loverti, V, Pakanen, VM, Tijsen, W & Kempenaers, B 2016, 'Unexpected diversity in socially synchronized rhythms of shorebirds', Nature, vol. 540, no. 7631, pp. 109-113. https://doi.org/10.1038/nature20563
Bulla M, Valcu M, Dokter AM, Dondua AG, Kosztolányi A, Rutten AL et al. Unexpected diversity in socially synchronized rhythms of shorebirds. Nature. 2016 Dec 1;540(7631):109-113. https://doi.org/10.1038/nature20563
Bulla, Martin ; Valcu, Mihai ; Dokter, Adriaan M. ; Dondua, Alexei G. ; Kosztolányi, András ; Rutten, Anne L. ; Helm, Barbara ; Sandercock, Brett K. ; Casler, Bruce ; Ens, Bruno J. ; Spiegel, Caleb S. ; Hassell, Chris J. ; Küpper, Clemens ; Minton, Clive ; Burgas, Daniel ; Lank, David B. ; Payer, David C. ; Loktionov, Egor Y. ; Nol, Erica ; Kwon, Eunbi ; Smith, Fletcher ; Gates, H. River ; Vitnerová, Hana ; Prüter, Hanna ; Johnson, James A. ; St Clair, James J H ; Lamarre, Jean François ; Rausch, Jennie ; Reneerkens, Jeroen ; Conklin, Jesse R. ; Burger, Joanna ; Liebezeit, Joe ; Bêty, Joël ; Coleman, Jonathan T. ; Figuerola, Jordi ; Hooijmeijer, Jos C E W ; Alves, José A. ; Smith, Joseph A M ; Weidinger, Karel ; Koivula, Kari ; Gosbell, Ken ; Exo, Klaus Michael ; Niles, Larry ; Koloski, Laura ; McKinnon, Laura ; Praus, Libor ; Klaassen, Marcel ; Giroux, Marie Andreé ; Sládecek, Martin ; Boldenow, Megan L. ; Goldstein, Michael I. ; Šálek, Miroslav ; Senner, Nathan ; Rönkä, Nelli ; Lecomte, Nicolas ; Gilg, Olivier ; Vincze, Orsolya ; Johnson, Oscar W. ; Smith, Paul A. ; Woodard, Paul F. ; Tomkovich, Pavel S. ; Battley, Phil F. ; Bentzen, Rebecca ; Lanctot, Richard B. ; Porter, Ron ; Saalfeld, Sarah T. ; Freeman, Scott ; Brown, Stephen C. ; Yezerinac, Stephen ; Székely, Tamás ; Montalvo, Tomás ; Piersma, Theunis ; Loverti, Vanessa ; Pakanen, Veli Matti ; Tijsen, Wim ; Kempenaers, Bart. / Unexpected diversity in socially synchronized rhythms of shorebirds. In: Nature. 2016 ; Vol. 540, No. 7631. pp. 109-113.
@article{637cf645c1d548a1a157401d39ea5564,
title = "Unexpected diversity in socially synchronized rhythms of shorebirds",
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.",
author = "Martin Bulla and Mihai Valcu and Dokter, {Adriaan M.} and Dondua, {Alexei G.} and Andr{\'a}s Kosztol{\'a}nyi and Rutten, {Anne L.} and Barbara Helm and Sandercock, {Brett K.} and Bruce Casler and Ens, {Bruno J.} and Spiegel, {Caleb S.} and Hassell, {Chris J.} and Clemens K{\"u}pper and Clive Minton and Daniel Burgas and Lank, {David B.} and Payer, {David C.} and Loktionov, {Egor Y.} and Erica Nol and Eunbi Kwon and Fletcher Smith and Gates, {H. River} and Hana Vitnerov{\'a} and Hanna Pr{\"u}ter and Johnson, {James A.} and {St Clair}, {James J H} and Lamarre, {Jean Fran{\cc}ois} and Jennie Rausch and Jeroen Reneerkens and Conklin, {Jesse R.} and Joanna Burger and Joe Liebezeit and Jo{\"e}l B{\^e}ty and Coleman, {Jonathan T.} and Jordi Figuerola and Hooijmeijer, {Jos C E W} and Alves, {Jos{\'e} A.} and Smith, {Joseph A M} and Karel Weidinger and Kari Koivula and Ken Gosbell and Exo, {Klaus Michael} and Larry Niles and Laura Koloski and Laura McKinnon and Libor Praus and Marcel Klaassen and Giroux, {Marie Andre{\'e}} and Martin Sl{\'a}decek and Boldenow, {Megan L.} and Goldstein, {Michael I.} and Miroslav Š{\'a}lek and Nathan Senner and Nelli R{\"o}nk{\"a} and Nicolas Lecomte and Olivier Gilg and Orsolya Vincze and Johnson, {Oscar W.} and Smith, {Paul A.} and Woodard, {Paul F.} and Tomkovich, {Pavel S.} and Battley, {Phil F.} and Rebecca Bentzen and Lanctot, {Richard B.} and Ron Porter and Saalfeld, {Sarah T.} and Scott Freeman and Brown, {Stephen C.} and Stephen Yezerinac and Tam{\'a}s Sz{\'e}kely and Tom{\'a}s Montalvo and Theunis Piersma and Vanessa Loverti and Pakanen, {Veli Matti} and Wim Tijsen and Bart Kempenaers",
year = "2016",
month = "12",
day = "1",
doi = "10.1038/nature20563",
language = "English",
volume = "540",
pages = "109--113",
journal = "Nature",
issn = "0028-0836",
publisher = "Nature Research",
number = "7631",

}

TY - JOUR

T1 - Unexpected diversity in socially synchronized rhythms of shorebirds

AU - Bulla, Martin

AU - Valcu, Mihai

AU - Dokter, Adriaan M.

AU - Dondua, Alexei G.

AU - Kosztolányi, András

AU - Rutten, Anne L.

AU - Helm, Barbara

AU - Sandercock, Brett K.

AU - Casler, Bruce

AU - Ens, Bruno J.

AU - Spiegel, Caleb S.

AU - Hassell, Chris J.

AU - Küpper, Clemens

AU - Minton, Clive

AU - Burgas, Daniel

AU - Lank, David B.

AU - Payer, David C.

AU - Loktionov, Egor Y.

AU - Nol, Erica

AU - Kwon, Eunbi

AU - Smith, Fletcher

AU - Gates, H. River

AU - Vitnerová, Hana

AU - Prüter, Hanna

AU - Johnson, James A.

AU - St Clair, James J H

AU - Lamarre, Jean François

AU - Rausch, Jennie

AU - Reneerkens, Jeroen

AU - Conklin, Jesse R.

AU - Burger, Joanna

AU - Liebezeit, Joe

AU - Bêty, Joël

AU - Coleman, Jonathan T.

AU - Figuerola, Jordi

AU - Hooijmeijer, Jos C E W

AU - Alves, José A.

AU - Smith, Joseph A M

AU - Weidinger, Karel

AU - Koivula, Kari

AU - Gosbell, Ken

AU - Exo, Klaus Michael

AU - Niles, Larry

AU - Koloski, Laura

AU - McKinnon, Laura

AU - Praus, Libor

AU - Klaassen, Marcel

AU - Giroux, Marie Andreé

AU - Sládecek, Martin

AU - Boldenow, Megan L.

AU - Goldstein, Michael I.

AU - Šálek, Miroslav

AU - Senner, Nathan

AU - Rönkä, Nelli

AU - Lecomte, Nicolas

AU - Gilg, Olivier

AU - Vincze, Orsolya

AU - Johnson, Oscar W.

AU - Smith, Paul A.

AU - Woodard, Paul F.

AU - Tomkovich, Pavel S.

AU - Battley, Phil F.

AU - Bentzen, Rebecca

AU - Lanctot, Richard B.

AU - Porter, Ron

AU - Saalfeld, Sarah T.

AU - Freeman, Scott

AU - Brown, Stephen C.

AU - Yezerinac, Stephen

AU - Székely, Tamás

AU - Montalvo, Tomás

AU - Piersma, Theunis

AU - Loverti, Vanessa

AU - Pakanen, Veli Matti

AU - Tijsen, Wim

AU - Kempenaers, Bart

PY - 2016/12/1

Y1 - 2016/12/1

N2 - 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.

AB - 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.

UR - http://www.scopus.com/inward/record.url?scp=85000613387&partnerID=8YFLogxK

U2 - 10.1038/nature20563

DO - 10.1038/nature20563

M3 - Article

VL - 540

SP - 109

EP - 113

JO - Nature

JF - Nature

SN - 0028-0836

IS - 7631

ER -