Hatching asynchrony as a reproductive strategy in birds may explain the hatching failure of the last eggs of the clutch

  1. Fuertes‐Recuero, Manuel 1
  2. Baldan, Davide 2
  3. Cantarero, Alejandro 1
  1. 1 Department of Physiology, Veterinary School Complutense University of Madrid Avenida Puerta de Hierro s/n 28040 Madrid Spain
  2. 2 Department of Biology University of Nevada Reno NV USA
Revista:
Ibis

ISSN: 0019-1019,  1474-919X

Any de publicació: 2024

Pàgines: 1-12

Tipus: Article

DOI: 10.1111/IBI.13354 GOOGLE SCHOLAR lock_openAccés obert editor

Altres publicacions en: Ibis

Resum

Hatching failure, due to infertility or embryo mortality, is an important factor contributing to reduced reproductive success in birds. Although hatching failure and its possible causes have been widely investigated, the stage of development at which embryo death occurs and its association with laying order have rarely been studied. The relative size of eggs laid in different positions within the laying order is a key factor that can lead to different parental reproductive strategies, such as hatching asynchrony. Here we investigate hatching failure in relation to laying order by establishing the developmental stage of dead embryos found in unhatched European Pied Flycatcher Ficedula hypoleuca eggs and considering possible causes of failure. We found that variation in egg dimensions showed a quadratic relationship with laying order, with relatively large volumes and sizes in the first and last positions of the clutch. Egg position in the laying sequence was also related to hatching failure, with the first and last positions being more susceptible to failure. The death of embryos late in development was more likely for eggs laid later in the sequence. To our knowledge, this is the first study showing that females may be adaptively allocating more resources to last-laid eggs to avoid competitive disadvantages between siblings, a strategy that seems to fail becasue these eggs suffer greater embryo mortality.

Referències bibliogràfiques

  • Anderson D.J., (1997), Funct. Ecol., 11, pp. 331, 10.1046/j.1365-2435.1997.00091.x
  • Arnold T.W., (1987), Am. Nat., 130, pp. 643, 10.1086/284736
  • Bates D., (2015), J. Stat. Softw., 67, pp. 1, 10.18637/jss.v067.i01
  • Birkhead T.R., (2008), Ibis, 150, pp. 508, 10.1111/j.1474-919X.2008.00813.x
  • Blackburn T.M., (1991), Auk, 108, pp. 973
  • Bolton M., (1991), J. Anim. Ecol., 60, pp. 949, 10.2307/5424
  • Briskie J.V., (2004), Proc. Natl. Acad. Sci. U. S. A., 101, pp. 558, 10.1073/pnas.0305103101
  • Cabezas‐Díaz S., (2007), Ardea, 95, pp. 55, 10.5253/078.095.0106
  • Canal D., (2011), Behaviour, 148, pp. 691, 10.1163/000579511X573917
  • Cantarero A., (2013), J. Avian Biol., 44, pp. 591, 10.1111/j.1600-048X.2013.00134.x
  • Cantarero A., (2014), Anim. Behav., 94, pp. 167, 10.1016/j.anbehav.2014.05.002
  • Clifford L.D., (2002), Behav. Ecol., 13, pp. 274, 10.1093/beheco/13.2.274
  • Clotfelter E.D., (2000), J. Avian Biol., 31, pp. 329, 10.1034/j.1600-048X.2000.310308.x
  • Cooke F., (1985), Evolution, 39, pp. 165
  • Cordero P.J., (1999), J. Avian Biol., 30, pp. 103, 10.2307/3677249
  • Di Giovanni A.J., (2023), Ornithology, 140, 10.1093/ornithology/ukac048
  • Enemar A., (1989), Ornis Fenn., 66, pp. 32
  • Forbes S., (1997), Nature, 390, pp. 351, 10.1038/37025
  • Graves J., (1992), Anim. Behav., 44, pp. 389, 10.1016/0003-3472(92)90047-D
  • Halekoh U.&Højsgaard S.2014.Pbkrtest: Parametric bootstrap and Kenward Roger based methods for mixed model comparison. R package version 0.4‐2.
  • Hartig F.2022.DHARMa: Residual Diagnostics for Hierarchical (Multi‐Level/Mixed) Regression Models. Available from:https://cran.r‐project.org/web/packages/DHARMa/vignettes/DHARMa.html
  • Hemmings N., (2016), Ibis, 158, pp. 43, 10.1111/ibi.12336
  • Hoyt D.F., (1979), Auk, 96, pp. 73
  • Jamieson I.G., (2000), Biol. Conserv., 94, pp. 107, 10.1016/S0006-3207(99)00158-5
  • Järvinen A., (1984), Auk, 101, pp. 439, 10.1093/auk/101.3.439
  • Jenni L., (1994), Moult and Ageing of European Passerines
  • Jeon J., (2008), Behav. Ecol., 19, pp. 344, 10.1093/beheco/arm136
  • Johnson L.S., (2009), J. Avian Biol., 40, pp. 248, 10.1111/j.1600-048X.2009.04777.x
  • Koenig W.D., (1982), Auk, 99, pp. 526
  • Kozlowski C.P., (2010), Gen. Comp. Endocrinol., 168, pp. 460, 10.1016/j.ygcen.2010.06.006
  • Krist M., (2011), Biol. Rev., 86, pp. 692, 10.1111/j.1469-185X.2010.00166.x
  • Leblanc Y., (1987), Can. J. Zool., 65, pp. 3044, 10.1139/z87-461
  • Lord A.M., (2011), J. Avian Biol., 42, pp. 187, 10.1111/j.1600-048X.2010.05256.x
  • Magrath R.D., (1992), J. Zool., 227, pp. 639, 10.1111/j.1469-7998.1992.tb04420.x
  • Meathrel C.E., (1993), Oecologia, 93, pp. 162, 10.1007/BF00317665
  • Monclús R., (2017), Oecologia, 185, pp. 629, 10.1007/s00442-017-3977-2
  • Moreno J., (2013), Ethology, 119, pp. 727, 10.1111/eth.12112
  • Morrow E.H., (2002), J. Evol. Biol., 15, pp. 702, 10.1046/j.1420-9101.2002.00445.x
  • Murton R.K., (1974), Ibis, 116, pp. 52, 10.1111/j.1474-919X.1974.tb00223.x
  • Ostreiher R., (1997), Behav. Ecol., 8, pp. 233, 10.1093/beheco/8.2.233
  • Ostreiher R., (2001), Behav. Ecol. Sociobiol., 49, pp. 340, 10.1007/s002650000308
  • Parsons J., (1970), Nature, 228, pp. 1221, 10.1038/2281221a0
  • Pettifor R.A., (2001), J. Anim. Ecol., 70, pp. 62, 10.1111/j.1365-2656.2001.00465.x
  • Pijanowski B.C., (1992), Am. Nat., 139, pp. 1270, 10.1086/285386
  • Pinowska B., (2002), Acta Ornithol., 37, pp. 7, 10.3161/068.037.0102
  • Pizzari T., (2000), Nature, 405, pp. 787, 10.1038/35015558
  • Potti J., (1996), Condor, 98, pp. 328, 10.2307/1369151
  • R Development Core Team.2017.R: a language and environment for statistical computing. Vienna Austria: R Foundation for Statistical Computing.
  • Reid W.V., (1990), Evolution, 44, pp. 1780, 10.2307/2409506
  • Robertson G.J., (1993), Can. J. Zool., 71, pp. 544, 10.1139/z93-075
  • Romanoff A.L., (1949), Auk, 66, pp. 264, 10.2307/4080357
  • Royle N.J., (1999), Funct. Ecol., 13, pp. 298, 10.1046/j.1365-2435.1999.00306.x
  • Ruiz‐De‐Castañeda R., (2012), The Condor, 114, pp. 203, 10.1525/cond.2011.100230
  • Serrano D., (2005), J. Avian Biol., 36, pp. 242, 10.1111/j.0908-8857.2005.03395.x
  • Siitari H., (2002), Behav. Ecol., 13, pp. 737, 10.1093/beheco/13.6.737
  • Sirkiä P.M., (2021), Ecol. Evol., 11, pp. 1501, 10.1002/ece3.7048
  • Slagsvold T., (1985), Ornis Scand., 16, pp. 81, 10.2307/3676471
  • Smith H.G., (1995), Ecology, 76, pp. 1, 10.2307/1940626
  • Soler M. Ruiz‐Raya F. Sánchez‐Pérez L.&Ibáñez‐Álamo J.D.2020.Parental feeding preferences rather than sibling competition determine the death of smaller nestlings in asynchronous broods.bioRxiv2020.12.01.404590. Available from:https://doi.org/10.1101/2020.12.01.404590
  • Spottiswoode C., (2004), Proc. Biol. Sci., 271, pp. 267, 10.1098/rspb.2003.2605
  • Stewart I.R.K., (2013), J. Avian Biol., 44, pp. 069, 10.1111/j.1600-048X.2012.05795.x
  • Stoleson S., (1999), Proc. 22 Int. Ornithol. Congr., Durban, pp. 600
  • Svensson L., (1984), Identification guide to European passerines
  • Temizyürek T., (2022), Ardea, 110, pp. 1, 10.5253/arde.2022.a6
  • Veiga J.P., (1992), Am. Nat., 139, pp. 669, 10.1086/285351
  • Veiga J., (1993), Ornis Scand., 24, pp. 237, 10.2307/3676739
  • Webb D.R., (1987), Condor, 89, pp. 874, 10.2307/1368537
  • Węgrzyn E., (2012), Ardea, 100, pp. 179, 10.5253/078.100.0209
  • Węgrzyn E., (2023), J. Ornithol., 164, pp. 477, 10.1007/s10336-023-02066-8
  • Wiebe K.L., (1996), Auk, 113, pp. 258, 10.2307/4088961
  • Williams T.D., (1993), Oikos, 67, pp. 250, 10.2307/3545469
  • Ylimaunu J., (1987), Ornis Fenn., 64, pp. 10