In birds, incubation by both parents is a common form of care for eggs. Although the involvement of the two parents may vary dramatically between and within pairs, as well as over the course of the day and breeding season, detailed descriptions of this variation are rare, especially in species with variable male contributions to care. Here, we continuously video-monitored 113 nests of Northern Lapwings Vanellus vanellus to reveal the diversity of incubation rhythms and parental involvement, as well as their daily and seasonal variation. We found great between-nest variation in the overall nest attendance (68-94%; median = 87%) and in how much males attended their nests (0-37%; median = 13%). Notably, the less the males attended their nests, the lower was the overall nest attendance, even though females partially compensated for the males' decrease. Also, despite seasonal environmental trends (e.g. increasing temperature), incubation rhythms changed little over the season and 27-day incubation period. However, as nights shortened with the progressing breeding season, the longest night incubation bout of females shortened too. Importantly, within the 24h-day, nest attendance was highest, incubation bouts longest, exchange gaps shortest and male involvement lowest during the night. Moreover, just after sunrise and before sunset males attended the nest the most. To conclude, we confirm substantial between nest differences in Lapwing male nest attendance, reveal how such differences relates to variation in incubation rhythms, and describe strong circadian incubation rhythms modulated by sunrise and sunset.

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

Faculty of Environmental Sciences Czech University of Life Sciences Prague Kamýcká 129 Praha Suchdol 165 00 Czech Republic

NIOZ Royal Netherlands Institute for Sea Research Department of Coastal Systems and Utrecht University P O Box 59 1790 AB Den Burg The Netherlands

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Hawkins M, Battaglia A. Breeding behaviour of the platypus (Ornithorhynchus anatinus) in captivity. Aust. J. Zool. 2009;57:283–293. doi: 10.1071/ZO09090. DOI

Hutchison VH, Dowling HG, Vinegar A. Thermoregulation in a brooding female Indian Python, Python molurus bivittatus. Science. 1966;151:694–696. doi: 10.1126/science.151.3711.694. PubMed DOI

Deeming, C. Behaviour patterns during incubation in Avian incubation: behaviour, environment and evolution (ed. Deeming, C.). 63–87 (Oxford University Press, 2002).

Kendeigh, S. C. Parental care and its evolution in birds. Illinois Biographical Monographs22, (Illinois Biographical Monographs, 1952).

Skutch AF. The incubation patterns of birds. Ibis. 1957;99:69–93. doi: 10.1111/j.1474-919X.1957.tb01934.x. DOI

Bulla M, et al. Unexpected diversity in socially synchronized rhythms of shorebirds. Nature. 2016;540:109–113. doi: 10.1038/nature20563. PubMed DOI

Johnstone RM, Davis LS. Incubation routines and foraging‐trip regulation in the Grey‐faced Petrel Pterodroma macroptera gouldi. Ibis. 1990;132:14–20. doi: 10.1111/j.1474-919X.1990.tb01011.x. DOI

Weimerskirch H. Regulation of foraging trips and incubation routine in male and female wandering albatrosses. Oecologia. 1995;102:37–43. doi: 10.1007/BF00333308. PubMed DOI

Gauthier-Clerc M, Le Maho Y, Gendner JP, Durant J, Handrich Y. State-dependent decisions in long-term fasting king penguins, Aptenodytes patagonicus, during courtship and incubation. Anim. Behav. 2001;62:661–669. doi: 10.1006/anbe.2001.1803. DOI

Grant GS. Avian incubation: egg temperature, nest humidity, and behavioral thermoregulation in a hot environment. Ornithol. Monogr. 1982;30:1–82.

Blanken MS, Nol E. Factors affecting parental behavior in Semipalmated Plovers. Auk. 1998;115:166–174. doi: 10.2307/4089121. DOI

Wiebe KL. Division of labour during incubation in a woodpecker Colaptes auratus with reversed sex roles and facultative polyandry. Ibis. 2008;150:115–124. doi: 10.1111/j.1474-919X.2007.00754.x. DOI

Bulla M, Valcu M, Rutten AL, Kempenaers B. Biparental incubation patterns in a high-Arctic breeding shorebird: how do pairs divide their duties? Behav. Ecol. 2014;25:152–164. doi: 10.1093/beheco/art098. PubMed DOI PMC

Bartlett TL, Mock DW, Schwagmeyer PL. Division of labor: incubation and biparental care in House Sparrows (Passer domesticus) Auk. 2005;122:835–842. doi: 10.1642/0004-8038(2005)122[0835:DOLIAB]2.0.CO;2. DOI

Coulson JC, Wooller RD. Incubation under natural conditions in the kittiwake gull, Rissa tridactyla. Anim. Behav. 1984;32:1204–1215. doi: 10.1016/S0003-3472(84)80238-9. DOI

Hawkins LL. Nesting behavior of male and female Whistling Swans and implications of male incubation. Wildfowl. 1986;37:5–27.

Afton AD. Factors Affecting Incubation Rhythms of Northern Shovelers. Condor. 1980;82:132–137. doi: 10.2307/1367462. DOI

Kleindorfer S, Fessl B, Hoi H. More is not always better: Male incubation in two Acrocephalus Warblers. Behaviour. 1995;132:607–625. doi: 10.1163/156853995X00234. DOI

Reid JM, Monaghan P, Ruxton GD. Males matter: The occurrence and consequences of male incubation in starlings (Sturnus vulgaris) Behav. Ecol. Sociobiol. 2002;51:255–261. doi: 10.1007/s00265-001-0435-1. DOI

Ospina EA, Cooper CB, Liljesthröm M, Ardia DR, Winkler DW. Biparental nest-attendance in Chilean Swallows (Tachycineta meyeni) breeding in Ushuaia, Argentina. Emu. 2015;115:76–79. doi: 10.1071/MU14036. DOI

Voss MA, Rutter MA, Zimmerman NG, Moll KM. Adaptive value of thermally inefficient male incubation in Barn Swallows (Hirundo rustica) Auk. 2008;125:637–642. doi: 10.1525/auk.2008.07046. DOI

Vincze O, et al. Local environment but not genetic differentiation influences biparental care in ten Plover populations. PLoS One. 2013;8:e60998. doi: 10.1371/journal.pone.0060998. PubMed DOI PMC

Vincze O, et al. Parental cooperation in a changing climate: fluctuating environments predict shifts in care division. Glob. Ecol. Biogeogr. 2016;26:347–358. doi: 10.1111/geb.12540. DOI

Bulla M, et al. Flexible parental care: Uniparental incubation in biparentally incubating shorebirds. Sci. Rep. 2017;7:12851. doi: 10.1038/s41598-017-13005-y. PubMed DOI PMC

Zhang L, et al. Biparental incubation pattern of the Black-necked Crane on an alpine plateau. J. Ornithol. 2017;158:697–705. doi: 10.1007/s10336-017-1439-6. DOI

Bambini, G., Schlicht, E. & Kempenaers, B. Patterns of female nest attendance and male feeding throughout the incubation period in Blue Tits Cyanistes caeruleus. Ibis. (2018).

Grønstøl GB. Mate-sharing costs in polygynous Northern Lapwings Vanellus vanellus. Ibis. 2003;145:203–211. doi: 10.1046/j.1474-919X.2003.00141.x. DOI

Jongbloed F, Schekkerman H, Teunissen W. Verdeling van de broedinspanning bij Kieviten. Limosa. 2006;79:63–70.

Liker A, Székely T. Parental behaviour in the Lapwing Vanellus vanellus. Ibis. 1999;141:608–614. doi: 10.1111/j.1474-919X.1999.tb07368.x. DOI

Lislevand T, et al. Incubation Behaviour in Northern Lapwings: Nocturnal Nest Attentiveness and Possible Importance of Individual Breeding Quality. Ethology. 2004;110:177–192. doi: 10.1111/j.1439-0310.2004.00967.x. DOI

Lislevand T, Byrkjedal I. Incubation behaviour in male Northern Lapwing Vanellus vanellus in relation to mating opportunities and female body condition. Ardea. 2004;92:19–30.

Reneerkens J, Grond K, Schekkerman H, Tulp I, Piersma T. Do uniparental sanderlings Calidris alba increase egg heat input to compensate for low nest attentiveness? PLoS One. 2011;6:e16834. doi: 10.1371/journal.pone.0016834. PubMed DOI PMC

Sládeček, M. & Bulla, M. Supporting information for ‘Diverse incubation rhythm in a facultatively uniparental shorebird - the Northern Lapwing’. Open Sci. Framew. http://osf.io/y4vpe (2018). PubMed PMC

Bulla, M. et al. Supporting Information for ‘Unexpected diversity in socially synchronized rhythms of shorebirds’. Open Sci. Framew. 10.17605/OSF.IO/WXUFM (2016). PubMed

Onrust J, Piersma T. The Hungry Worm Feeds the Bird. Ardea. 2017;105:153–161. doi: 10.5253/arde.v105i2.a4. DOI

Onrust J, et al. Detection of earthworm prey by Ruff Philomachus pugnax. Ibis. 2017;159:647–656. doi: 10.1111/ibi.12467. DOI

Weidinger K. Foraging behaviour of nest predators at open-cup nests of woodland passerines. J. Ornithol. 2010;151:729–735. doi: 10.1007/s10336-010-0512-1. DOI

Praus L, Weidinger K. Predators and nest success of Sky Larks Alauda arvensis in large arable fields in the Czech Republic. Bird Study. 2010;57:525–530. doi: 10.1080/00063657.2010.506208. DOI

Hegyi Z, Sasvari L. Components of fitness in Lapwings Vanellus vanellus and Black-tailed Godwits Limosa limosa during the breeding season: Do female body mass and egg size matter? Ardea. 1998;86:43–50.

Hegyi Z. Laying date, egg volumes and chick survival in Lapwing (Vanellus vanellus L.), Redshank (Tringa totanus L.), and black tailed Godwit (Limosa limosa L.) Ornis Hungarica. 1996;6:1–7.

Byrkjedal I, Kålås JA. Seasonal variation in egg size in golden plover Pluvialis apricaria and dotterel Charadrius morinellus populations. Ornis Scand. 1985;16:108–112. doi: 10.2307/3676475. DOI

Løfaldli L. Incubation rhythm in the Great Snipe Gallinago media. Holarct. Ecol. 1985;8:107–112.

Kålås JA. Incubation schedules in different parental systems in the Dotterel Charadrius morinellus. Ardea. 1986;74:185–190.

Carter AW, Hopkins WA, Moore IT, Durant SE. Influence of incubation recess patterns on incubation period and hatchling traits in wood ducks Aix sponsa. J. Avian Biol. 2014;45:273–279. doi: 10.1111/j.1600-048X.2013.00275.x. DOI

Bueno-Enciso J, Barrientos R, Ferrer ES, Sanz JJ. Do extended incubation recesses carry fitness costs in two cavity-nesting birds? J. F. Ornithol. 2017;88:146–155. doi: 10.1111/jofo.12194. DOI

Hepp GR, Kennamer RA, Johnson MH. Maternal effects in Wood Ducks: Incubation temperature influences incubation period and neonate phenotype. Funct. Ecol. 2006;20:307–314. doi: 10.1111/j.1365-2435.2006.01108.x. DOI

Amininasab SM, Birker M, Kingma SA, Hildenbrandt H, Komdeur J. The effect of male incubation feeding on female nest attendance and reproductive performance in a socially monogamous bird. J. Ornithol. 2017;158:687–696. doi: 10.1007/s10336-016-1427-2. DOI

Bolton M. Determinants of chick survival in the Lesser Black-Backed Gull: relative contributions of egg size and parental quality. J. Anim. Ecol. 1991;60:949–960. doi: 10.2307/5424. DOI

Blomqvist D, Johansson OC, Götmark F. Parental quality and egg size affect chick survival in a precocial bird, the lapwing Vanellus vanellus. Oecologia. 1997;110:18–24. doi: 10.1007/s004420050128. PubMed DOI

Parish DMB, Coulson JC. Parental investment, reproductive success and polygyny in the lapwing, Vanellus vanellus. Anim. Behav. 1998;56:1161–1167. doi: 10.1006/anbe.1998.0856. PubMed DOI

Lislevand T. Male incubation in Northern Lapwings: effects on egg temperature and potential benefits to females. Ornis Fenn. 2001;78:23–29.

Székely T, Cuthill IC. Trade-off between mating opportunities and parental care: brood desertion by female Kentish plovers. Proc. Biol. Sci. 2000;267:2087–2092. doi: 10.1098/rspb.2000.1253. PubMed DOI PMC

Dunn PO, Robertson RJ. Geographic variation in the importance of male parental care and mating systems in tree swallows. Behav. Ecol. 1992;3:291–299. doi: 10.1093/beheco/3.4.291. DOI

Whittingham LA, Robertson RJ. Food Availability, Parental Care and Male Mating Success in Red-Winged Blackbirds (Agelaius phoeniceus) J. Anim. Ecol. 1994;63:139–150. doi: 10.2307/5590. DOI

Kis J, Liker A, Székely T. Nest defence by Lapwings: Observation on natural behaviour and an experiment. Ardea. 2000;88:155–164.

Šálek M. Polygamous breeding of Northern Lapwings (Vanellus vanellus) in southern Bohemia, Czech Republic. Sylvia. 2005;41:72–82.

Smith HG, Sandell MI, Bruun M. Paternal care in the European starling, Sturnus vulgaris: incubation. Anim. Behav. 1995;50:323–331. doi: 10.1006/anbe.1995.0248. DOI

Silver R, Andrews H, Ball GF, Andrews H, Ball F. Parental Care in an Ecological Perspective: A Quantitative Analysis of Avian Subfamilies. Am. Zool. 1985;25:823–840. doi: 10.1093/icb/25.3.823. DOI

Jónsson JE, Afton AD, Alisauskas RT. Does body size influence nest attendance? A comparison of Ross’s geese (Chen rossii) and the larger, sympatric lesser snow geese (C. caerulescens caerulescens) J. Ornithol. 2007;148:549–555. doi: 10.1007/s10336-007-0169-6. DOI

Bulla, M., Valcu, M., Rutten, A. L. & Kempenaers, B. Temporary mate removal during incubation leads to variable compensation in a biparental shorebird. BioRxiv 1–24 (2017).

Harrison F, Barta Z, Cuthill I, Székely T. How is sexual conflict over parental care resolved? A meta-analysis. J. Evol. Biol. 2009;22:1800–1812. doi: 10.1111/j.1420-9101.2009.01792.x. PubMed DOI

McNamara JM, Gasson CE, Houston AI. Incorporating rules for responding into evolutionary games. Nature. 1999;401:368–371. PubMed

McNamara JM, Houston AI, Barta Z, Osorno JL. Should young ever be better off with one parent than with two? Behav. Ecol. 2003;14:301–310. doi: 10.1093/beheco/14.3.301. DOI

Houston AI, Székely T, McNamara JM. Conflict between parents over care. Trends Ecol. Evol. 2005;20:33–38. doi: 10.1016/j.tree.2004.10.008. PubMed DOI

Jones K, Ruxton G, Monaghan P. Model parents: is full compensation for reduced partner nest attendance compatible with stable biparental care? Behav. Ecol. 2002;13:838–843. doi: 10.1093/beheco/13.6.838. DOI

Pedler RD, Weston MA, Bennett ATD. Long incubation bouts and biparental incubation in the nomadic Banded Stilt. Emu. 2015;116:75–80. doi: 10.1071/MU15061. DOI

Reneerkens J, Piersma T, Sinninghe Damsté JS. Switch to diester preen waxes may reduce avian nest predation by mammalian predators using olfactory cues. J. Exp. Biol. 2005;208:4199–4202. doi: 10.1242/jeb.01872. PubMed DOI

Ward D. Incubation Temperatures and Behavior of Crowned, Black-Winged, and Lesser Black-Winged Plovers. Auk. 1990;107:10–17.

Zerba E, Morton ML. The rhythm of incubation from egg laying to hatching in Mountain White-crowned Sparrows. Ornis Scand. 1983;14:188–197. doi: 10.2307/3676152. DOI

Gillings S, Sutherland WJ. Comparative Diurnal and Nocturnal Diet and Foraging in Eurasian Golden Plovers Pluvialis apricaria and Northern Lapwings Vanellus vanellus Wintering on Arable Farmland. Ardea. 2007;95:243–257. doi: 10.5253/078.095.0207. DOI

Ntiamoa-Baidu Y, et al. Water depth selection, daily feeding routines and diets of waterbirds in coastal lagoons in Ghana. Ibis. 2008;140:89–103. doi: 10.1111/j.1474-919X.1998.tb04545.x. DOI

Cardilini APA, Weston MA, Dann P, Sherman CDH. Sharing the Load: Role Equity in the Incubation of a Monomorphic Shorebird, the Masked Lapwing (Vanellus miles) Wilson J. Ornithol. 2015;127:730–733. doi: 10.1676/14-189. DOI

Ekanayake KB, et al. The bright incubate at night: sexual dichromatism and adaptive incubation division in an open-nesting shorebird. Proc. R. Soc. Lon. B. 2015;282:20143026. doi: 10.1098/rspb.2014.3026. PubMed DOI PMC

Meissner W, Wójcik C, Pinchuk P, Karlionova N. Ageing and sexing the Northern Lapwing Vanellus vanellus. Wader Study Gr. Bull. 2013;120:32–36.

von Blotzheim, G. Handbuch der Vögel MitteleuropasBand 6: Charadriiformes (1. Teil). 445-470 (AULA-Verlag, 1999).

Warnock N, Oring LW. Nocturnal Nest Attendance of Killdeers: More Than Meets the Eye. Auk. 1996;113:502–504. doi: 10.2307/4088919. DOI

Thibault M, McNeil R. Day- and night-time parental investment by incubating Wilson’s Plovers in a tropical environment. Can. J. Zool. 1995;73:879–886. doi: 10.1139/z95-103. DOI

St Clair JJH, Herrmann P, Woods RW, Székely T. Female-biased incubation and strong diel sex-roles in the Two-banded Plover Charadrius falklandicus. J. Ornithol. 2010;151:811–816. doi: 10.1007/s10336-010-0517-9. DOI

Lessells CM, McNamara JM. Sexual conflict over parental investment in repeated bouts: negotiation reduces overall care. Proc. R. Soc. B Biol. Sci. 2012;279:1506–1514. doi: 10.1098/rspb.2011.1690. PubMed DOI PMC

Williams, B. Energetics of avian incubation in Avian energetics and nutritional ecology (ed. Carey, C.). 375-416 (Chapman & Hall, 1996).

Van Paassen AG, Veldman DH, Beintema AJ. A simple device for determination of incubation stages in eggs. Wildfowl. 1984;35:173–178.

Šálek M. Frequent within-pair copulations during incubation in Northern Lapwings Vanellus vanellus are consistent with the sperm competition hypothesis. J. Ornithol. 2015;156:737–742. doi: 10.1007/s10336-015-1179-4. DOI

Schonert B, Byrkjedal I, Lislevand T. Plumage ornaments in male Northern Lapwings Vanellus vanellus may not be a reliable indicator of their mating success. Ornis Fenn. 2014;91:79–87.

Byrkjedal I, Grønstøl G, Lislevand T. Mating systems and territory in Lapwings Vanellus vanellus. Ibis (Lond. 1859). 1997;139:129–137. doi: 10.1111/j.1474-919X.1997.tb04512.x. DOI

Liker A, Székely T. Mating pattern and mate choice in the Lapwing Vanellus vanellus. Zoology. 1999;8–9:13–25.

R-Core-Team. R: A Language and Environment for Statistical Computing. http://www.r-project.org/ (2017).

Bates D, et al. Fitting Linear Mixed-Effects Models Using lme4. J. Stat. Softw. 2015;67:1–48. doi: 10.18637/jss.v067.i01. DOI

Nakagawa S, Schielzeth H. Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol. Rev. Camb. Philos. Soc. 2010;85:935–56. PubMed

Schielzeth H. Simple means to improve the interpretability of regression coefficients. Methods Ecol. Evol. 2010;1:103–113. doi: 10.1111/j.2041-210X.2010.00012.x. DOI

Gelman, A. et al. Data Analysis Using Regression and Multilevel/Hierarchical Models. CRAN Repository 1–53. https://cran.r-project.org/package=arm (2016).

Offspring thermal demands and parental brooding efficiency differ for precocial birds living in contrasting climates

Diel timing of nest predation changes across breeding season in a subtropical shorebird

Parental incubation exchange in a territorial bird species involves sex-specific signalling

Diversity of incubation rhythms in a facultatively uniparental shorebird - the Northern Lapwing