Search

Menu
Search
in Ecology

Reduced chick performance makes supernormal clutches maladaptive in a shorebird

25 Views


Abstract

Life-history theory predicts a trade-off between the number and quality of offspring, and that clutch sizes may be adjusted in relation to environmental conditions. In many bird species, however, clutch size is remarkably consistent, in which case factors constraining clutch size evolution are more debated. A classic example is found in shorebirds (Charadriiformes), where clutch size is typically fixed at four eggs across species and environments. Here, we experimentally enlarged clutches of Common Ringed Plovers Charadrius hiaticula to test the hypothesis that clutch sizes are constrained by parental incubation capacity. While most previous tests of this idea compared hatching success between clutch sizes, often with mixed results, we also investigated potential post-hatching effects. We found that chicks from enlarged clutches were consistently smaller during the first two weeks of their lives and showed higher mortality rates compared to control chicks. Although hatching success was relatively unaffected, enlarged clutches experienced reduced mass loss indicating slower embryonic growth, required longer incubation periods and hatched more asynchronously than controls. These findings suggest that laying an extra egg would be a waste of resources, with negative effects outweighing potential benefits. Our results highlight the potential importance of previously overlooked post-hatching constraints in shaping clutch size evolution in shorebirds.

Similar content being viewed by others

Warming Arctic summers unlikely to increase productivity of shorebirds through renesting

Article
Open access
27 July 2021

Impact of embryonic manipulations on core body temperature dynamics and survival in broilers exposed to cyclic heat stress

Article
Open access
06 September 2022

Reproductive individuality of clonal fish raised in near-identical environments and its link to early-life behavioral individuality

Article
Open access
24 November 2023

Data availability

The data and code generated during the current study have been archived in Figshare, https://doi.org/10.6084/m9.figshare.29715869.

References

  1. Lack, D. The significance of clutch-size. Ibis 89, 302–352 (1947).

    Google Scholar 

  2. Monaghan, P. & Nager, R. G. Why don’t birds Lay more eggs? Trends Ecol. Evol. 12, 270–274. https://doi.org/10.1016/s0169-5347(97)01094-x (1997).

    Google Scholar 

  3. Both, C., Tinbergen, J. M. & van Noordwijk, A. J. Offspring fitness and individual optimization of clutch size. Proceedings of the Royal Society B 265, 2303–2307 (1998). https://doi.org/10.1098/rspb.1998.0575

  4. Roff, D. A. Evolution of Life Histories: Theory and Analysis 1 edn (Springer, 1992).

  5. Stearns, S. C. The Evolution of Life Histories (Oxford University Press, 1992).

  6. Lundblad, C. G. & Conway, C. J. Nest microclimate and limits to egg viability explain avian life-history variation across latitudinal gradients. Ecology 102, e03338 (2021).

    Google Scholar 

  7. Martin, T. E., Martin, P. R., Olson, C. R., Heidinger, B. J. & Fontaine, J. J. Parental care and clutch sizes in North and South American birds. Science 287, 1482–1485. https://doi.org/10.1126/science.287.5457.1482 (2000).

    Google Scholar 

  8. Sibly, R. M. et al. Energetics, lifestyle, and reproduction in birds. Proc. Natl. Acad. Sci. 109, 10937–10941. https://doi.org/10.1073/pnas.1206512109 (2012).

    Google Scholar 

  9. Walters, J. R. in In Behavior of Marine Animals. Volume 5. Shorebirds: Breeding Behavior and Populations. 5, 243–287 (eds Joanna, Burger, Bori, L. & Olla) (Plenum, 1984).

  10. Arnold, T. W. What limits clutch size in waders? J. Avian Biol. 30, 216–220. https://doi.org/10.2307/3677131 (1999).

    Google Scholar 

  11. Hope, S. F. et al. Incubation temperature as a constraint on clutch size evolution. Funct. Ecol. 35, 909–919 (2021).

    Google Scholar 

  12. Deeming, D. C. Avian Incubation: Behaviour, Environment, and Evolution (Oxford University Press, 2001).

  13. DuRant, S. E., Hopkins, W. A., Hepp, G. R. & Walters, J. R. Ecological, evolutionary, and conservation implications of incubation temperature-dependent phenotypes in birds. Biol. Rev. 88, 499–509. https://doi.org/10.1111/brv.12015 (2013).

    Google Scholar 

  14. DuRant, S. E., Hopkins, W. A. & Hepp, G. R. Embryonic developmental patterns and energy expenditure are affected by incubation temperature in wood ducks (Aix sponsa). Physiol. Biochem. Zool.: Ecol. Evolut. Approaches. 84, 451–457 (2011).

    Google Scholar 

  15. Ar, A. & Rahn, H. Water in the avian egg: overall budget of incubation. Am. Zool. 20, 373–384. https://doi.org/10.1093/icb/20.2.373 (1980).

    Google Scholar 

  16. Booth, D. T. & Rahn, H. Factors modifying rate of water loss from birds’ eggs during incubation. Physiol. Zool. 63, 697–709 (1990).

    Google Scholar 

  17. Deeming, D. C. & Ferguson, M. W. J. in Egg Incubation: its Effects on Embryonic Development in Birds and Reptiles. 147–172 (eds Deeming, D. C. & Ferguson, M. W. J.) (Cambridge University Press, 1991).

  18. Ton, R. & Martin, T. E. Proximate effects of temperature versus evolved intrinsic constraints for embryonic development times among temperate and tropical songbirds. Sci. Rep. 7 https://doi.org/10.1038/s41598-017-00885-3 (2017).

  19. Hepp, G. R., DuRant, S. E. & Hopkins, W. A. in Nests, Eggs, & Incubation. New Ideas about Avian Reproduction. 171–178 (eds Deeming, D. C. & Reynolds, S. J.) (Oxford University Press, 2015).

  20. Eiby, Y. A. & Booth, D. T. The effects of incubation temperature on the morphology and composition of Australian Brush-turkey (Alectura lathami) chicks. J. Comp. Physiol. B: Biochem. Systemic Environ. Physiol. 179, 875–882. https://doi.org/10.1007/s00360-009-0370-4 (2009).

    Google Scholar 

  21. Hepp, G. R. & Kennamer, R. A. Warm is better: incubation temperature influences apparent survival and recruitment of wood ducks (Aix sponsa). PLoS One. 7, e47777. https://doi.org/10.1371/journal.pone.0047777 (2012).

    Google Scholar 

  22. DuRant, S., Hopkins, W., Carter, A., Stachowiak, C. & Hepp, G. Incubation conditions are more important in determining early thermoregulatory ability than posthatch resource conditions in a precocial bird. Physiol. Biochem. Zool. 86, 410–420. https://doi.org/10.1086/671128 (2013).

    Google Scholar 

  23. Nord, A. & Nilsson, J. Å. Incubation temperature affects growth and energy metabolism in blue tit nestlings. Am. Nat. 178, 639–651. https://doi.org/10.1086/662172 (2011).

    Google Scholar 

  24. Wada, H. et al. Transient and permanent effects of suboptimal incubation temperatures on growth, metabolic rate, immune function and adrenocortical responses in zebra finches. J. Exp. Biol. 218, 2847–2855. https://doi.org/10.1242/jeb.114108 (2015).

    Google Scholar 

  25. Pakanen, V. M. et al. Low frequencies of supernormal clutches in the Southern Dunlin and the temminck’s stint. Ardea 107, 61–74. (2019).

    Google Scholar 

  26. Larsen, V. A., Lislevand, T. & Byrkjedal, I. Is clutch size limited by incubation ability in Northern lapwings? J. Anim. Ecol. 72, 784–792 (2003).

    Google Scholar 

  27. Lengyel, S., Kiss, B. & Tracy, C. R. Clutch size determination in shorebirds: revisiting incubation limitation in the pied Avocet (Recurvirostra avosetta). J. Anim. Ecol. 78, 396–405. https://doi.org/10.1111/j.1365-2656.2008.01486.x (2009).

    Google Scholar 

  28. Wallander, J. & Andersson, M. Clutch size limitation in waders: experimental test in redshank Tringa Totanus. Oecologia 130, 391–395. https://doi.org/10.1007/s004420100812 (2002).

    Google Scholar 

  29. Olson, C. R., Vleck, C. M. & Vleck, D. Periodic cooling of bird eggs reduces embryonic growth efficiency. Physiol. Biochem. Zool. 79, 927–936. https://doi.org/10.1086/506003 (2006).

    Google Scholar 

  30. Székely, T., Karsai, I. & Williams, T. Determination of clutch-size in the Kentish plover Charadrius Alexandrinus. Ibis 136, 341–348 (1994).

    Google Scholar 

  31. Wallander, J. & Andersson, M. Reproductive tactics of the ringed plover Charadrius hiaticula. J. Avian Biol. 34, 259–266. https://doi.org/10.1034/j.1600-048X.2003.03109.x (2003).

    Google Scholar 

  32. Pienkowski, M. W. Behaviour of young ringed plovers Charadrius hiaticula and its relationship to growth and survival to reproductive age. Ibis 126, 133–155 (1984).

    Google Scholar 

  33. Wanders, K. et al. Incubation behaviour of the common ringed plover Charadrius hiaticula. J. Ornithol. 164, 825–833. https://doi.org/10.1007/s10336-023-02077-5 (2023).

    Google Scholar 

  34. Liebezeit, J. R. et al. Assessing the development of shorebird eggs using the flotation method: species-specific and generalized regression models. Condor 109, 32–47 (2007).

    Google Scholar 

  35. Reid, J. M., Monaghan, P. & Ruxton, G. D. The consequences of clutch size for incubation conditions and hatching success in starlings. Funct. Ecol. 14, 560–565 (2000).

    Google Scholar 

  36. Meissner, W., Chylarecki, P. & Skakuj, M. Ageing and sexing the ringed plover Charadrius hiaticula. Wader Study Group. Bull. 117, 99–102 (2010).

    Google Scholar 

  37. Busse, P. & Meissner, W. Bird Ringing Station Manual (De Gruyter Open Ltd, 2015).

  38. Bruford, M. W., Hanotte, O., Brookfield, J. F. Y. & Burke, T. in Molecular Genetic Analysis of Populations. A Practical Approach. 287–336 (eds Hoelzel, A. R.) (Oxford University Press, 1998).

  39. van der Velde, M., Haddrath, O., Verkuil, Y. I., Baker, A. J. & Piersma, T. New primers for molecular sex identification of waders. Wader Study. 124, 147–151. https://doi.org/10.18194/ws.00069 (2017).

    Google Scholar 

  40. R Development Core Team. R: a Language and Environment for Statistical Computing (Vienna, 2021).

  41. Bates, D., Maechler, M., Bolker, B. & Walker, S. Fitting linear mixed-effect models using lme4. J. Stat. Softw. 67, 1–48. https://doi.org/10.18637/jss.v067.i01 (2015).

    Google Scholar 

  42. Väisänen, R. A., Hildén, O., Soikkeli, M. & Vuolanto, S. Egg dimension variation in five wader species: the role of heredity. Ornis Fennica. 49, 25–44 (1972).

    Google Scholar 

  43. Laake, J. & RMark R code for mark analysis. 3.0.0 (2022). https://cran.r-project.org/web/packages/RMark/RMark.pdf

  44. Therneau, T. A package for survival analysis in R. R package version 3.2–13 (2021). https://CRAN.R-project.org/package=survival

  45. Burnham, K. P. & Anderson, D. R. Multimodel inference: Understanding AIC and BIC in model selection. Sociol. Methods Res. 33, 261–304 (2004).

    Google Scholar 

  46. Arnold, T. W. Uninformative parameters and model selection using akaike’s information criterion. J. Wildl. Manage. 74, 1175–1178. https://doi.org/10.1111/j.1937-2817.2010.tb01236.x (2010).

    Google Scholar 

  47. Sutherland, C. et al. Practical advice on variable selection and reporting using Akaike information criterion. Proc. Royal Soc. B. 290, 20231261. https://doi.org/10.1098/rspb.2023.1261 (2023).

    Google Scholar 

  48. Thomson, D. L., Monaghan, P. & Furness, R. W. The demands of incubation and avian clutch size. Biol. Rev. 73, 293–304. https://doi.org/10.1111/j.1469-185X.1998.tb00032.x (1998).

    Google Scholar 

  49. Niizuma, Y., Takagi, M., Senda, M., Chochi, M. & Watanuki, Y. Incubation capacity limits maximum clutch size in Black-tailed gulls Larus crassirostris. J. Avian Biol. 36, 421–427. https://doi.org/10.1111/j.0908-8857.2005.03252.x (2005).

    Google Scholar 

  50. Yogev, A., Ar, A. & Yom-Tov, Y. Determination of clutch size and the breeding biology of the Spur-winged plover (Vanellus spinosus) in Israel. Auk 113, 68–73 (1996).

    Google Scholar 

  51. Ardia, D. R., Pérez, J. H. & Clotfelter, E. D. Experimental cooling during incubation leads to reduced innate immunity and body condition in nestling tree swallows. Proceedings of the Royal Society B 277, 1881–1888 (2010). https://doi.org/10.1098/rspb.2009.2138

  52. Grant, M. C. Relationships between egg size, chick size at hatching, and chick survival in the whimbrel Numenius Phaeopus. Ibis 133, 111–225. https://doi.org/10.1111/j.1474-919X.1991.tb04823.x (1991).

    Google Scholar 

  53. Krist, M. Egg size and offspring quality: a meta-analysis in birds. Biol. Rev. 86, 692–716. https://doi.org/10.1111/j.1469-185X.2010.00166.x (2011).

    Google Scholar 

  54. Booth, D. T. & Jones, D. N. in Avian Incubation: Behaviour, Environment and Evolution. 192–206 (eds Deeming, D. C.) (Oxford University Press, 2001).

  55. Klaassen, M., Slagsvold, G. & Bech, C. Metabolic rate and thermostability in relation to availability of yolk in hatchlings of Black-legged Kittiwake and domestic chicken. Auk 104, 787–789. https://doi.org/10.1093/auk/104.4.787 (1987).

    Google Scholar 

  56. Visser, G. H. & Ricklefs, R. E. Relationships between body composition and homeothermy in neonates of precocial and semiprecocial birds. Auk 112, 192–200. https://doi.org/10.2307/4088778 (1995).

    Google Scholar 

  57. Hötker, H. Conspecific nest parasitism in the pied Avocet Recurvirostra Avosetta. Ibis 142, 280–288 (2000).

    Google Scholar 

  58. Cooper, C. B., Hochachka, W. M., Phillips, T. B. & Dhondt, A. A. Geographical and seasonal gradients in hatching failure in Eastern bluebirds Sialia Sialis reinforce clutch size trends. Ibis 148, 221–230 (2006).

    Google Scholar 

  59. Metcalfe, N. B. & Monaghan, P. Compensation for a bad start: grow now, pay later? Trends Ecol. Evol. 16, 254–260. https://doi.org/10.1016/S0169-5347(01)02124-3 (2001).

    Google Scholar 

  60. DuRant, S., Hopkins, W., Wilson, A. & Hepp, G. Incubation temperature affects the metabolic cost of thermoregulation in a young precocial bird. Funct. Ecol. 26, 416–422. https://doi.org/10.1111/j.1365-2435.2011.01945.x (2012).

    Google Scholar 

  61. Visser, G. H. & Ricklefs, R. E. Temperature regulation in neonates of shorebirds. Auk 110, 445–457. https://doi.org/10.2307/4088409 (1993).

    Google Scholar 

  62. Schekkerman, H. & Boele, A. Foraging in precocial chicks of the Black-tailed godwit Limosa limosa: vulnerability to weather and prey size. J. Avian Biol. 40, 369–379. https://doi.org/10.1111/j.1600-048X.2008.04330.x (2009).

    Google Scholar 

  63. DuRant, S. E., Hopkins, W. A., Hawley, D. M. & Hepp, G. R. Incubation temperature affects multiple measures of immunocompetence in young wood ducks (Aix sponsa). Biol. Lett. 8, 108–111. https://doi.org/10.1098/rsbl.2011.0735 (2011).

    Google Scholar 

  64. DuRant, S., Hepp, G., Moore, I., Hopkins, B. & Hopkins, W. Slight differences in incubation temperature affect early growth and stress endocrinology of wood Duck (Aix sponsa) ducklings. J. Exp. Biol. 213, 45–51. https://doi.org/10.1242/jeb.034488 (2010).

    Google Scholar 

  65. Nager, R. G., Monaghan, P. & Houston, D. C. Within-clutch trade-offs between the number and quality of eggs: experimental manipulations in gulls. Ecology 81, 1339–1350. https://doi.org/10.1890/0012-9658(2000)081[1339:Wctobt]2.0.Co;2 (2000).

    Google Scholar 

  66. Safriel, U. N. On the significance of clutch size in nidifugous birds. Ecology 56, 703–708 (1975).

    Google Scholar 

Download references

Acknowledgements

We are grateful to Thomas Lameris for valuable help in the field and for statistical support. We also thank Freya Coursey for field assistance, and Tamás Székely for supporting parts of the field work and laboratory analyses.

Funding

Open access funding provided by University of Bergen. The study was funded by the Meltzer Research Fund, BirdLife Norway, Statoil’s Research Fund/Nansen Fund, the County Governor of Troms & Finnmark, and the Natural Environment Research Council (NE/S007504/1).

Author information

Authors and Affiliations

  1. Department of Natural History, University Museum of Bergen, University of Bergen, Bergen, Norway

    Oddvar Heggøy & Terje Lislevand

  2. Natural History Museum of Denmark, University of Copenhagen, Copenhagen, Denmark

    Kees Wanders

  3. Department of Life Sciences, Milner Centre for Evolution, University of Bath, Bath, UK

    Kees Wanders

Authors

  1. Oddvar Heggøy
    View author publications

    Search author on:PubMed Google Scholar

  2. Kees Wanders
    View author publications

    Search author on:PubMed Google Scholar

  3. Terje Lislevand
    View author publications

    Search author on:PubMed Google Scholar

Contributions

O.H. planned, organized and carried out fieldwork, collected and analysed the data and wrote the manuscript. K.W. participated in data collection and performed molecular sexing. T.L. conceived the study, planned and carried out fieldwork, supervised research and edited the manuscript. All authors substantially contributed to the content of the paper.

Corresponding author

Correspondence to
Oddvar Heggøy.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary Material 1

Rights and permissions

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.

Reprints and permissions

About this article

Cite this article

Heggøy, O., Wanders, K. & Lislevand, T. Reduced chick performance makes supernormal clutches maladaptive in a shorebird.
Sci Rep (2026). https://doi.org/10.1038/s41598-026-37872-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1038/s41598-026-37872-6

Keywords

  • Incubation limitation hypothesis
  • Clutch size evolution
  • Precocial birds
  • Shorebirds
  • Postnatal effects

Source: Ecology - nature.com

A unified plant ecology database for Spain

Linking aerobic scope to fitness in the wild reveals potential opportunities to help recover imperiled salmon populations

This portal is not a newspaper as it is updated without periodicity. It cannot be considered an editorial product pursuant to law n. 62 of 7.03.2001. The author of the portal is not responsible for the content of comments to posts, the content of the linked sites. Some texts or images included in this portal are taken from the internet and, therefore, considered to be in the public domain; if their publication is violated, the copyright will be promptly communicated via e-mail. They will be immediately removed.

Back to Top
Close