Unexpected diversity in socially synchronized rhythms of shorebirds

M. Bulla; M. Valcu; A.M. Dokter; A.G. Dondua; A. Kosztolányi; A.L. Rutten; B. Helm; B.K. Sandercock; B. Casler; B.J. Ens; C.S. Spiegel; C.J. Hassell; C. Küpper; C. Minton; D. Burgas; D.B. Lank; D.C. Payer; E.Y. Loktionov; E. Nol; E. Kwon; F. Smith; H.R. Gates; H. Vitnerová; H. Prüter; J.A. Johnson; James St Clair; J.F. Lamarre; J. Rausch; J. Reneerkens; J.R. Conklin; J. Burger; J. Liebezeit; J. Bêty; J.T. Coleman; J. Figuerola; J.C.E.W. Hooijmeijer; J.A. Alves; J.A.M. Smith; K. Weidinger; K. Koivula; K. Gosbell; K.M. Exo; L. Niles; L. Koloski; L. Mckinnon; L. Praus; M. Klaassen; M.A. Giroux; M. Sládecek; M.L. Boldenow; M.I. Goldstein; M. Šálek; N. Senner; N. Rönkä; N. Lecomte; O. Gilg; O. Vincze; O.W. Johnson; P.A. Smith; P.F. Woodard; P.S. Tomkovich; P.F. Battley; R. Bentzen; R.B. Lanctot; R. Porter; S.T. Saalfeld; S. Freeman; S.C. Brown; S. Yezerinac; T. Székely; T. Montalvo; T. Piersma; V. Loverti; V.M. Pakanen; W. Tijsen; B. Kempenaers

doi:10.1038/nature20563

Unexpected diversity in socially synchronized rhythms of shorebirds

M. Bulla, M. Valcu, A.M. Dokter, A.G. Dondua, A. Kosztolányi, A.L. Rutten, B. Helm, B.K. Sandercock, B. Casler, B.J. Ens, C.S. Spiegel, C.J. Hassell, C. Küpper, C. Minton, D. Burgas, D.B. Lank, D.C. Payer, E.Y. Loktionov, E. Nol, E. KwonF. Smith, H.R. Gates, H. Vitnerová, H. Prüter, J.A. Johnson, James St Clair, J.F. Lamarre, J. Rausch, J. Reneerkens, J.R. Conklin, J. Burger, J. Liebezeit, J. Bêty, J.T. Coleman, J. Figuerola, J.C.E.W. Hooijmeijer, J.A. Alves, J.A.M. Smith, K. Weidinger, K. Koivula, K. Gosbell, K.M. Exo, L. Niles, L. Koloski, L. Mckinnon, L. Praus, M. Klaassen, M.A. Giroux, M. Sládecek, M.L. Boldenow, M.I. Goldstein, M. Šálek, N. Senner, N. Rönkä, N. Lecomte, O. Gilg, O. Vincze, O.W. Johnson, P.A. Smith, P.F. Woodard, P.S. Tomkovich, P.F. Battley, R. Bentzen, R.B. Lanctot, R. Porter, S.T. Saalfeld, S. Freeman, S.C. Brown, S. Yezerinac, T. Székely, T. Montalvo, T. Piersma, V. Loverti, V.M. Pakanen, W. Tijsen, B. Kempenaers

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103 Citations (Scopus)

Abstract

© 2016 Macmillan Publishers Limited. All rights reserved.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 language	English
Pages (from-to)	109-113
Number of pages	5
Journal	Nature
Volume	540
Issue number	7631
DOIs	https://doi.org/10.1038/nature20563
Publication status	Published - 1 Dec 2016

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Bulla, M., Valcu, M., Dokter, A. M., Dondua, A. G., Kosztolányi, A., Rutten, A. L., Helm, B., Sandercock, B. K., Casler, B., Ens, B. J., Spiegel, C. S., Hassell, C. J., Küpper, C., Minton, C., Burgas, D., Lank, D. B., Payer, D. C., Loktionov, E. Y., Nol, E., ... Kempenaers, B. (2016). Unexpected diversity in socially synchronized rhythms of shorebirds. Nature, 540(7631), 109-113. https://doi.org/10.1038/nature20563

@article{6ed3c26a54734d0cb9f80e98d975cdcb,

title = "Unexpected diversity in socially synchronized rhythms of shorebirds",

abstract = "{\textcopyright} 2016 Macmillan Publishers Limited. All rights reserved.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 = "M. Bulla and M. Valcu and A.M. Dokter and A.G. Dondua and A. Kosztol{\'a}nyi and A.L. Rutten and B. Helm and B.K. Sandercock and B. Casler and B.J. Ens and C.S. Spiegel and C.J. Hassell and C. K{\"u}pper and C. Minton and D. Burgas and D.B. Lank and D.C. Payer and E.Y. Loktionov and E. Nol and E. Kwon and F. Smith and H.R. Gates and H. Vitnerov{\'a} and H. Pr{\"u}ter and J.A. Johnson and {St Clair}, James and J.F. Lamarre and J. Rausch and J. Reneerkens and J.R. Conklin and J. Burger and J. Liebezeit and J. B{\^e}ty and J.T. Coleman and J. Figuerola and J.C.E.W. Hooijmeijer and J.A. Alves and J.A.M. Smith and K. Weidinger and K. Koivula and K. Gosbell and K.M. Exo and L. Niles and L. Koloski and L. Mckinnon and L. Praus and M. Klaassen and M.A. Giroux and M. Sl{\'a}decek and M.L. Boldenow and M.I. Goldstein and M. {\v S}{\'a}lek and N. Senner and N. R{\"o}nk{\"a} and N. Lecomte and O. Gilg and O. Vincze and O.W. Johnson and P.A. Smith and P.F. Woodard and P.S. Tomkovich and P.F. Battley and R. Bentzen and R.B. Lanctot and R. Porter and S.T. Saalfeld and S. Freeman and S.C. Brown and S. Yezerinac and T. Sz{\'e}kely and T. Montalvo and T. Piersma and V. Loverti and V.M. Pakanen and W. Tijsen and B. Kempenaers",

year = "2016",

month = dec,

day = "1",

doi = "10.1038/nature20563",

language = "English",

volume = "540",

pages = "109--113",

journal = "Nature",

issn = "0028-0836",

publisher = "Nature Publishing Group - Macmillan Publishers",

number = "7631",

}

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, J, 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

TY - JOUR

T1 - Unexpected diversity in socially synchronized rhythms of shorebirds

AU - Bulla, M.

AU - Valcu, M.

AU - Dokter, A.M.

AU - Dondua, A.G.

AU - Kosztolányi, A.

AU - Rutten, A.L.

AU - Helm, B.

AU - Sandercock, B.K.

AU - Casler, B.

AU - Ens, B.J.

AU - Spiegel, C.S.

AU - Hassell, C.J.

AU - Küpper, C.

AU - Minton, C.

AU - Burgas, D.

AU - Lank, D.B.

AU - Payer, D.C.

AU - Loktionov, E.Y.

AU - Nol, E.

AU - Kwon, E.

AU - Smith, F.

AU - Gates, H.R.

AU - Vitnerová, H.

AU - Prüter, H.

AU - Johnson, J.A.

AU - St Clair, James

AU - Lamarre, J.F.

AU - Rausch, J.

AU - Reneerkens, J.

AU - Conklin, J.R.

AU - Burger, J.

AU - Liebezeit, J.

AU - Bêty, J.

AU - Coleman, J.T.

AU - Figuerola, J.

AU - Hooijmeijer, J.C.E.W.

AU - Alves, J.A.

AU - Smith, J.A.M.

AU - Weidinger, K.

AU - Koivula, K.

AU - Gosbell, K.

AU - Exo, K.M.

AU - Niles, L.

AU - Koloski, L.

AU - Mckinnon, L.

AU - Praus, L.

AU - Klaassen, M.

AU - Giroux, M.A.

AU - Sládecek, M.

AU - Boldenow, M.L.

AU - Goldstein, M.I.

AU - Šálek, M.

AU - Senner, N.

AU - Rönkä, N.

AU - Lecomte, N.

AU - Gilg, O.

AU - Vincze, O.

AU - Johnson, O.W.

AU - Smith, P.A.

AU - Woodard, P.F.

AU - Tomkovich, P.S.

AU - Battley, P.F.

AU - Bentzen, R.

AU - Lanctot, R.B.

AU - Porter, R.

AU - Saalfeld, S.T.

AU - Freeman, S.

AU - Brown, S.C.

AU - Yezerinac, S.

AU - Székely, T.

AU - Montalvo, T.

AU - Piersma, T.

AU - Loverti, V.

AU - Pakanen, V.M.

AU - Tijsen, W.

AU - Kempenaers, B.

PY - 2016/12/1

Y1 - 2016/12/1

N2 - © 2016 Macmillan Publishers Limited. All rights reserved.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 - © 2016 Macmillan Publishers Limited. All rights reserved.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.

U2 - 10.1038/nature20563

DO - 10.1038/nature20563

M3 - Article

C2 - 27880762

SN - 0028-0836

VL - 540

SP - 109

EP - 113

JO - Nature

JF - Nature

IS - 7631

ER -

Unexpected diversity in socially synchronized rhythms of shorebirds

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