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title Unexpected diversity in socially synchronized rhythms of shorebirds
authors Bulla, M; Valcu, M; Dokter, AM; Dondua, AG; Kosztolanyi, A; Rutten, AL; Helm, B; Sandercock, BK; Casler, B; Ens, BJ; Spiegel, CS; Hassell, CJ; Kupper, C; Minton, C; Burgas, D; Lank, DB; Payer, DC; Loktionov, EY; Nol, E; Kwon, E; Smith, F; Gates, HR; Vitnerova, H; Pruter, H; Johnson, JA; St Clair, JJH; Lamarre, JF; Rausch, J; Reneerkens, J; Conklin, JR; Burger, J; Liebezeit, J; Bety, 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; Sladecek, M; Boldenow, ML; Goldstein, MI; Salek, M; Senner, N; Ronka, 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; Szekely, T; Montalvo, T; Piersma, T; Loverti, V; Pakanen, VM; Tijsen, W; Kempenaers, B
author full name Bulla, Martin; Valcu, Mihai; Dokter, Adriaan M. .; Dondua, Alexei G.; Kosztolanyi, Andras; Rutten, Anne L.; Helm, Barbara; Sandercock, Brett K.; Casler, Bruce; Ens, Bruno J.; Spiegel, Caleb S.; Hassell, Chris J.; Kuepper, Clemens; Minton, Clive; Burgas, Daniel; Lank, David B.; Payer, David C.; Loktionov, Egor Y.; Nol, Erica; Kwon, Eunbi; Smith, Fletcher; Gates, H. River; Vitnerova, Hana; Prueter, Hanna; Johnson, James A.; St Clair, James J. H.; Lamarre, Jean-Francois; Rausch, Jennie; Reneerkens, Jeroen; Conklin, Jesse R. .; Burger, Joanna; Liebezeit, Joe; Bety, Joel; Coleman, Jonathan T.; Figuerola, Jordi; Hooijmeijer, Jos C. . E. . W.; Alves, Jose 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-Andree; Sladecek, Martin; Boldenow, Megan L.; Goldstein, Michael I.; Salek, Miroslav; Senner, Nathan; Ronka, 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; Szekely, Tamas; Montalvo, Tomas; Piersma, Theunis; Loverti, Vanessa; Pakanen, Veli-Matti; Tijsen, Wim; Kempenaers, Bart
title Unexpected diversity in socially synchronized rhythms of shorebirds
nationality internacional
source NATURE
language English
document type Article
keywords plus INCUBATION PATTERNS; CIRCADIAN-RHYTHMS; SEXUAL SELECTION; GEOLOCATOR DATA; NEST PREDATION; PHYLOGENIES; BIRDS; EVOLUTION; CLOCKS; ROLES
abstract The behavioural rhythms of organisms are thought to be under strong selection, influenced by the rhythmicity of the environment(1-4). Such behavioural rhythms are well studied in isolated individuals under laboratory conditions(1,5), but free-living individuals have to temporally synchronize their activities with those of others, including potential mates, competitors, prey and predators(6-10). 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)(6-9,11). The behavioural rhythms that emerge from such social synchronization and the underlying evolutionary and ecological drivers that shape them remain poorly understood(5-7,9). Here we investigate these rhythms in the context of biparental care, a particularly sensitive phase of social synchronization(12) 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(5-7,9). The risk of predation, not the risk of starvation, may be a key factor underlying the diversity in these rhythms.
author address [Bulla, Martin; Valcu, Mihai; Rutten, Anne L.; Kempenaers, Bart] Max Planck Inst Ornithol, Dept Behav Ecol & Evolutionary Genet, Eberhard Gwinner Str, D-82319 Seewiesen, Germany; [Dokter, Adriaan M. .] Univ Amsterdam, Inst Biodivers & Ecosystem Dynam, Computat Geo Ecol, Sci Pk 904, NL-1098 XH Amsterdam, Netherlands; [Dondua, Alexei G.] Gatchinskaya,Apartment 27, St Petersburg 197198, Russia; [Kosztolanyi, Andras] Univ Vet Med Budapest, Dept Ecol, Rottenbiller U 50, H-1077 Budapest, Hungary; [Kosztolanyi, Andras; Vincze, Orsolya] Univ Debrecen, Dept Evolutionary Zool, MTA DE Lendulet Behav Ecol Res Grp, H-4032 Debrecen, Hungary; [Rutten, Anne L.] Apiloa GmbH, D-82319 Starnberg, Germany; [Helm, Barbara] Univ Glasgow, Inst Biodivers Anim Hlth & Comparat Med, Graham Kerr Bldg, Glasgow G12 8QQ, Lanark, Scotland; [Sandercock, Brett K.] Kansas State Univ, Div Biol, 116 Ackert Hall, Manhattan, KS 66506 USA; [Casler, Bruce] POB 1094, Fallon, NV 89407 USA; [Ens, Bruno J.] Sovon Dutch Ctr Field Ornithol, Coastal Ecol Team, POB 59, NL-1790 AB Den Burg, Texel, Netherlands; [Spiegel, Caleb S.] US Fish & Wildlife Serv, Div Migratory Birds, 300 Westgate Ctr Dr, Hadley, MA 01035 USA; [Hassell, Chris J.] Global Flyway Network, POB 3089, Broome, Western Austral 6725, Australia; [Kuepper, Clemens] Graz Univ, Inst Zool, Univ Pl 2, A-8010 Graz, Austria; [Minton, Clive] Victorian Wader Study Grp, 165 Dalgetty Rd, Melbourne, Vic, Australia; [Burgas, Daniel] Univ Helsinki, Dept Forest Sci, POB 27, FI-00014 Helsinki, Finland; [Burgas, Daniel] Univ Jyvaskyla, Dept Biol & Environm Sci, POB 35, FI-40014 Jyvaskyla, Finland; [Lank, David B.] Simon Fraser Univ, Dept Biol Sci, 8888 Univ Dr, Burnaby V5A 1S6, BC V5A 1S6, Canada; [Payer, David C.] Natl Pk Serv, Alaska Reg, 240 W 5th Ave, Anchorage, AK 99501 USA; [Loktionov, Egor Y.] Bauman Moscow State Tech Univ, State Lab Photon Energet, 2nd Baumanskaya St,5-1, Moscow 105005, Russia; [Nol, Erica] Trent Univ, Biol Dept, 2140 East Bank Dr, Peterborough K9L 0G2, ON, Canada; [Kwon, Eunbi] Virginia Polytech Inst & State Univ, Dept Fish & Wildlife Conservat, 310 West Campus Dr, Blacksburg, VA 24061 USA; [Smith, Fletcher] Virginia Commonwealth Univ, POB 8795, Williamsburg, VA USA; [Smith, Fletcher] Coll William & Mary, Ctr Conservat Biol, POB 8795, Williamsburg, VA USA; [Gates, H. River] Pacific Ecol Serv, 17520 Snow Crest Lane, Anchorage, AK 99516 USA; [Gates, H. River; Johnson, James A.; Lanctot, Richard B. .; Saalfeld, Sarah T.] US Fish & Wildlife Serv, Migratory Bird Management, 1011 East Tudor Rd, Anchorage, AK 99503 USA; [Gates, H. River; Brown, Stephen C. .] Shorebird Recovery Program, POB 545, Saxtons River, VT 05154 USA; [Vitnerova, Hana] Charles Univ Prague, Fac Sci, Albertov 6, Prague 12843, Czech Republic; [Prueter, Hanna] Leibniz Inst Zoo & Wildlife Res, Dept Wildlife Dis, Alfred Kowalke Str 17, D-10315 Berlin, Germany; [St Clair, James J. H.] Univ Bath, Dept Biol & Biochem, Biodivers Lab, Bath BA1 7AY, Avon, England; [St Clair, James J. H.] Univ Western Australia, Ctr Evolutionary Biol, Sch Biol, Stirling Highway, Crawley, Western Austral 6009, Australia; [Lamarre, Jean-Francois; Bety, Joel] Univ Quebe Rimouski, Dept Biol Chim & Geographie, 300 Alle Ursulines, Rimouski G5L 3A1, PQ G5L 3A1, Canada; [Lamarre, Jean-Francois; Bety, Joel] Univ Quebe Rimouski, CEN, 300 Alle Ursulines, Rimouski, PQ G5L 3A1, Canada; [Rausch, Jennie; Woodard, Paul F.] Environm & Climate Change Canada, Canadian Wildlife Serv, POB 2310,5019-52nd St,4th Floor, Yellowknife X1A 2P7, NT, Canada; [Reneerkens, Jeroen; Conklin, Jesse R. .; Hooijmeijer, Jos C. . E. . W.; Senner, Nathan; Piersma, Theunis] Univ Groningen, Groningen Inst Evolutionary Life Sci, Conservat Ecol Grp, Nijenborgh 7, NL-9747 AG Groningen, Netherlands; [Burger, Joanna] Rutgers State Univ, Div Life Sci, 604-Allison Rd, Piscataway, NJ 08854 USA; [Liebezeit, Joe] Audubon Soc Portland, 5151 NW Cornell Rd, Portland, OR 97210 USA; [Coleman, Jonathan T.] Queensland Wader Study Grp, 22 Parker St, Brisbane, Qld 4128, Australia; [Figuerola, Jordi] CSIC, Donana Biol Stn, Dept Wetland Ecol, Ave Amer Vespucio,S-N, Seville 41092, Spain; [Alves, Jose A.] Univ Aveiro, Dept Biol, Ctr Environm & Marine Studies CESAM, Campus Santiago, P-3810193 Aveiro, Portugal; [Alves, Jose A.] Univ Iceland, South Iceland Res Ctr, IS-800 Fjolheimar, Selfoss, Iceland; [Smith, Joseph A. M. .] LJ Niles Associates, POB 784, Cape May, NJ 08204 USA; [Weidinger, Karel; Praus, Libor] Palacky Univ, Dept Zool & Lab Ornithol, 17 Listopadu 50, Olomouc 77146, Czech Republic; [Koivula, Kari; Ronka, Nelli; Pakanen, Veli-Matti] Univ Oulu, Dept Ecol, POB 3000, Oulu 90014, Finland; [Gosbell, Ken] Australasian Wader Studies Grp, 1-19 Baldwin Rd, Melbourne, Vic, Australia; [Exo, Klaus-Michael] Inst Avian Res, Vogelwarte Helgoland, Vogelwarte 21, D-26386 Wilhelmshaven, Germany; [Niles, Larry] LJ Niles Associates, 109 Market Lane, Greenwich, CT 08323 USA; [Koloski, Laura] Trent Univ, Environm & Life Sci, 1600 West Bank Dr, Peterborough, ON K0L 0G2, Canada; [McKinnon, Laura] York Univ Glendon Campus, Bilingual Biol Program, 2275 Bayview Ave, Toronto, ON M4N 3M6, Canada; [Klaassen, Marcel] Deakin Univ, Ctr Integrat Ecol, 75 Pigdons Rd, Geelong, Vic 3216, Australia; [Giroux, Marie-Andree] Univ Quebec Rimouski, Canada Res Northern Biodivers, 300,Allee Ursulines, Rimouski, PQ G5L 3A8, Canada; [Giroux, Marie-Andree] Univ Quebec Rimouski, Ctr Etudes Nord, 300,Allee Ursulines, Rimouski, PQ G5L 3A8, Canada; [Giroux, Marie-Andree; Lecomte, Nicolas] Univ Moncton, Canada Res Polar & Boreal Ecol, 18 Ave Antonine Maillet, Moncton, NB E4K 1A6, Canada; [Giroux, Marie-Andree; Lecomte, Nicolas] Univ Moncton, Ctr Etudes Nord, 18 Ave Antonine Maillet, Moncton, NB E4K 1A6, Canada; [Sladecek, Martin; Salek, Miroslav] Czech Univ Life Sci Prague, Fac Environm Sci, Kamyck 1176, Prague 16521, Czech Republic; [Boldenow, Megan L.] Univ Alaska Fairbanks, Dept Biol & Wildlife, POB 756100, Fairbanks, AK 99775 USA; [Goldstein, Michael I.] Univ Alaska Southeast, Alaska Coastal Rainforest Ctr, 11120 Glacier Hwy, Juneau, AK 99801 USA; [Senner, Nathan] Cornell Lab Ornithol, 159 Sapsucker Woods Rd, Ithaca, NY 14850 USA; [Gilg, Olivier] Univ Bourgogne Franche Comte, Equipe Ecol Evolut, UMR Biogeosci 6282, 6 Bd Gabriel, F-21000 Dijon, France; [Gilg, Olivier] Grp Rech Ecol Arct, 16 Rue Vernot, F-21440 Francheville, France; [Vincze, Orsolya] Babes Bolyai Univ, Hungarian Dept Biol & Ecol, Evolutionary Ecol Grp, Clinicilor 5-7, RO-400006 Cluj Napoca, Romania; [Johnson, Oscar W.] Montana State Univ, Dept Ecol, Bozeman, MT 59717 USA; [Smith, Paul A.] Environm & Climate Change Canada, Wildlife Res Div, 1125 Colonel Dr, Ottawa, ON K1A 0H3, Canada; [Tomkovich, Pavel S.] Lomonosov Moscow State Univ, Zool Museum, Bolshaya Nikitskaya St 6, Moscow 125009, Russia; [Battley, Phil F.] Massey Univ, Inst Agr Environm, Private Bag 11 222, Palmerston North 4442, New Zealand; [Bentzen, Rebecca] Arctic Beringia Program, Wildlife Conservat Soc, 925 Schloesser Dr, Fairbanks, AK 99709 USA; [Porter, Ron] Delaware Bay Shorebird Project, Ambler, PA 19002 USA; [Freeman, Scott] US Fish & Wildlife Serv, Arctic Natl Wildlife Refuge, 101 12th Ave, Fairbanks, AK 99701 USA; [Yezerinac, Stephen] Fieldday Consulting, Surrey, BC V4N 6M5, Canada; [Szekely, Tamas] Univ Bath, Dept Biol & Biochem, Milner Ctr Evolut, Claverton, Bath BA2 7AY, Avon, England; [Montalvo, Tomas] Agencia Salut Publ Barcelona, Serv Vigilancia & Control Plagues Urbanes, Ave Princep Asturies 63, Barcelona 8012, Spain; [Piersma, Theunis] NIOZ Royal Netherlands, Inst Sea Res, Dept Coastal Syst, POB 59, NL-1790 AB Den Burg, Texel, Netherlands; [Piersma, Theunis] Univ Utrecht, POB 59, NL-1790 AB Den Burg, Texel, Netherlands; [Loverti, Vanessa] US Fish & Wildlife Serv, Migratory Bird & Habitat Program, 911 NE 11th Ave, Portland, OR 97232 USA; [Tijsen, Wim] Poelweg 12, NL-1778 KB Westerland, Netherlands
reprint address Bulla, M; Kempenaers, B (reprint author), Max Planck Inst Ornithol, Dept Behav Ecol & Evolutionary Genet, Eberhard Gwinner Str, D-82319 Seewiesen, Germany.
e-mail address bulla.mar@gmail.com; b.kempenaers@orn.mpg.de
funding agency and grant number Max Planck Society
funding text 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.
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cited reference count 72
times cited 1
total times cited count (wos, bci, and cscd) 1
publisher NATURE PUBLISHING GROUP
publisher city LONDON
publisher address MACMILLAN BUILDING, 4 CRINAN ST, LONDON N1 9XW, ENGLAND
issn 0028-0836
29-character source abbreviation NATURE
iso source abbreviation Nature
publication date DEC 1
year published 2016
volume 540
issue 7631
beginning page 109
ending page +
digital object identifier (doi) 10.1038/nature20563
page count 17
web of science category Multidisciplinary Sciences
subject category Science & Technology - Other Topics
document delivery number ED5UA
unique article identifier WOS:000388916600058
link http://www.nature.com/nature/journal/v540/n7631/full/nature20563.html
CESAM authors