Behavioral Ecology and Sociobiology

, Volume 68, Issue 2, pp 309–319 | Cite as

Is natural hatching asynchrony optimal? An experimental investigation of sibling competition patterns in a facultatively siblicidal seabird

  • Thomas MerklingEmail author
  • Lena Agdere
  • Elise Albert
  • Romain Durieux
  • Scott A. Hatch
  • Etienne Danchin
  • Pierrick Blanchard
Original Paper


In unpredictable environments, any tactic that enables avian parents to adjust brood size and, thus, energy expenditure to environmental conditions should be favoured. Hatching asynchrony (HA), which occurs whenever incubation commences before clutch completion, may comprise such a tactic. For instance, the sibling rivalry hypothesis states that the hierarchy among chicks, concomitant to HA, should both facilitate the adjustment of brood size to environmental conditions and reduce several components of sibling competition as compared to synchronous hatching, at both brood and individual levels. We thus predicted that brood aggression, begging and feeding rates should decrease and that older chick superiority should increase with HA increasing, leading to higher growth and survival rates. Accordingly, we investigated the effects of an experimental upward and downward manipulation of HA magnitude on behaviour, growth and survival of black-legged kittiwake (Rissa tridactyla) chicks. In line with the sibling rivalry hypothesis, synchronous hatching increased aggression and tended to increase feeding rates by parents at the brood level. Begging rates, however, increased with HA contrary to our expectations. At the individual level, as HA magnitude increased, the younger chick was attacked and begged proportionally more often, experienced a slower growth and a higher mortality than its sibling. Overall, the occurrence of energetic costs triggered by synchronous hatching both for parents and chicks, together with the lower growth rate and increased mortality of the younger chick in highly asynchronous broods suggest that natural HA magnitude may be optimal.


Aggression Begging Hatching asynchrony Kittiwake Sibling competition Sibling rivalry hypothesis 



We thank J.-B. Ferdy and F. Helfenstein for their statistical advice. We also thank J. White, an anonymous referee, and the associate editor Ian Hartley for their critical comments on earlier versions of the manuscript. The study was financed within a 4-year grant from the French Polar Institute Paul-Emile Victor (IPEV ‘Programme 1162 SexCoMonArc’). This work originated in the lab EDB, part of the ‘Laboratoire d'Excellence’ (LABEX) entitled TULIP (ANR-10-LABX-41).

Ethical standards

This experiment was conducted under the approval of the USGS Alaska Science Center Animal Care and Use Committee, the IPEV Ethical Committee, in accordance with U.S. laws and under permits from the U.S. Fish and Wildlife Service and the State of Alaska. Any use of trade names is for descriptive purposes only and does not imply endorsement of the U.S. Government.


  1. Altmann J (1974) Observational study of behavior: sampling methods. Behaviour 49:3–4CrossRefGoogle Scholar
  2. Anderson DJ (1989) The role of hatching asynchrony in siblicidal brood reduction of two booby species. Behav Ecol Sociobiol 25:363–368CrossRefGoogle Scholar
  3. Barrett RT, Runde OJ (1980) Growth and survival of nestling kittiwakes Rissa tridactyla in Norway. Ornis Scand 11:228–235CrossRefGoogle Scholar
  4. Bates D, Maechler M, Bolker BM (2011) package “lme4”: linear mixed-effects models using S4 classes (version 0.999375-42).
  5. Benowitz-Fredericks ZM, Kitaysky AS, Welcker J, Hatch SA (2013) Effects of food availability on yolk androgen deposition in the black-legged kittiwake (Rissa tridactyla), a seabird with facultative brood reduction. PLoS ONE 8:e62949PubMedCentralPubMedCrossRefGoogle Scholar
  6. Blanchard P, Hanuise N, Dano S, Weimerskirch H (2007) Offspring sex ratio in relation to parental structural size and body condition in the long-lived wandering albatross (Diomedea exulans). Behav Ecol Sociobiol 61:767–773CrossRefGoogle Scholar
  7. Box G, Cox D (1964) An analysis of transformations. J R Stat Soc B Met 26:211–252Google Scholar
  8. Braun BM, Hunt GLJ (1983) Brood reduction in black-legged kittiwakes. Auk 100:469–476Google Scholar
  9. Drent RH, Daan S (1980) The prudent parent: energetic adjustments in avian breeding. Ardea 68:225–252Google Scholar
  10. Drummond H (2006) Dominance in vertebrate broods and litters. Q Rev Biol 81:3–32PubMedCrossRefGoogle Scholar
  11. Drummond H, Gonzalez E, Osorno JL (1986) Parent–offspring cooperation in the blue-footed boody (Sula nebouxii): social roles in infanticial brood reduction. Behav Ecol Sociobiol 19:365–372CrossRefGoogle Scholar
  12. Drummond H, Rodriguez C, Schwabl H (2008) Do mothers regulate facultative and obligate siblicide by differentially provisioning eggs with hormones? J Avian Biol 39:139–143CrossRefGoogle Scholar
  13. Forbes LS (1991) Hunger and food allocation among nestlings of facultatively siblicidal ospreys. Behav Ecol Sociobiol 29:189–195CrossRefGoogle Scholar
  14. Forbes S (2011) Social rank governs the effective environment of siblings. Biol Lett 7:346–348PubMedCentralPubMedCrossRefGoogle Scholar
  15. Forbes S, Glassey B (2000) Asymmetric sibling rivalry and nestling growth in red-winged blackbirds (Agelaius phoeniceus). Behav Ecol Sociobiol 48:413–417CrossRefGoogle Scholar
  16. Forbes S, Thornton S, Glassey B, Forbes M, Buckley NJ (1997) Why parent birds play favourites. Nature 390:351–352CrossRefGoogle Scholar
  17. Fujioka M (1985) Sibling competition and siblicide in asynchronously-hatching broods of the cattle egret Bubulcus ibis. Anim Behav 33:1228–1242CrossRefGoogle Scholar
  18. Gilby AJ, Mainwaring MC, Griffith SC (2011) The adaptive benefit of hatching asynchrony in wild zebra finches. Anim Behav 82:479–484CrossRefGoogle Scholar
  19. Gill VA, Hatch SA (2002) Components of productivity in black-legged kittiwakes Rissa tridactyla: response to supplemental feeding. J Avian Biol 33:113–126CrossRefGoogle Scholar
  20. Gill VA, Hatch SA, Lanctot R (2002) Sensitivity of breeding parameters to food supply in black-legged kittiwakes Rissa tridactyla. Ibis 144:268–283CrossRefGoogle Scholar
  21. Godfray HCJ (1995) Signaling of need between parents and young: parent-offspring conflict and sibling rivalry. Am Nat 146:1–24CrossRefGoogle Scholar
  22. Hahn DC (1981) Asynchronous hatching in the laughing gull: cutting losses and reducing rivalry. Anim Behav 29:421–427CrossRefGoogle Scholar
  23. Hamilton WD (1964) The genetical evolution of social behaviour. I. J Theor Biol 7:1–16PubMedCrossRefGoogle Scholar
  24. Hatch SA, Robertson GJ, Baird HP (2009) Black-legged kittiwake (Rissa tridactyla). The birds of North America online. Cornell Laboratory of Ornithology, Ithaca, NYGoogle Scholar
  25. Hussell DJ (1972) Factors affecting clutch size in arctic passerines. Ecol Monogr 42:317–364CrossRefGoogle Scholar
  26. Irons DB (1992) Aspects of foraging behavior and reproductive biology of the black-legged kittiwake. University of California, IrvineGoogle Scholar
  27. Lack D (1947) The significance of clutch-size. Ibis 89:302–352CrossRefGoogle Scholar
  28. Lack D (1954) The natural regulation of animal numbers. Oxford University Press, OxfordGoogle Scholar
  29. Leclaire S, Helfenstein F, Degeorges A, Wagner RH, Danchin É (2010) Family size and sex-specific parental effort in black-legged kittiwakes. Behaviour 147:13–14CrossRefGoogle Scholar
  30. Leclaire S, Bourret V, Wagner RH, Hatch SA, Helfenstein F, Chastel O, Danchin É (2011) Behavioral and physiological responses to male handicap in chick-rearing black-legged kittiwakes. Behav Ecol 22:1156–1165CrossRefGoogle Scholar
  31. Magrath RD (1990) Hatching asynchrony in altricial birds. Biol Rev 65:587–622CrossRefGoogle Scholar
  32. Mainwaring MC, Blount JD, Hartley IR (2012) Hatching asynchrony can have long-term consequences for offspring fitness in zebra finches under captive conditions. Biol J Linn Soc 106:430–438CrossRefGoogle Scholar
  33. Maynard-Smith J (1982) Evolution and the theory of games. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  34. Maynard-Smith J, Parker GA (1976) The logic of asymmetric contests. Anim Behav 24:159–175CrossRefGoogle Scholar
  35. Merkling T, Leclaire S, Danchin E, Lhuillier E, Wagner RH, White J, Hatch SA, Blanchard P (2012) Food availability and offspring sex in a monogamous seabird: insights from an experimental approach. Behav Ecol 23:751–758CrossRefGoogle Scholar
  36. Mock DW (1994) Brood reduction: narrow sense, broad sense. J Avian Biol 25:3–7CrossRefGoogle Scholar
  37. Mock DW, Forbes LS (1994) Life-history consequences of avian brood reduction. Auk 111:115–123CrossRefGoogle Scholar
  38. Mock DW, Parker GA (1997) The evolution of sibling rivalry. Oxford University Press, OxfordGoogle Scholar
  39. Mock DW, Ploger BJ (1987) Parental manipulation of optimal hatch asynchrony in cattle egrets: an experimental study. Anim Behav 35:150–160CrossRefGoogle Scholar
  40. Mock DW, Schwagmeyer PL (1990) The peak load reduction hypothesis for avian hatching asynchrony. Evol Ecol 4:249–260CrossRefGoogle Scholar
  41. Müller MS, Roelofs Y, Erikstad KE, Groothuis TG (2012) Maternal androgens increase sibling aggression, dominance, and competitive ability in the siblicidal black-legged kittiwake (Rissa tridactyla). PloS ONE 7:e47763PubMedCentralPubMedCrossRefGoogle Scholar
  42. Nathan A, Legge S, Cockburn A (2001) Nestling aggression in broods of a siblicidal kingfisher, the laughing kookaburra. Behav Ecol 12:716–725CrossRefGoogle Scholar
  43. Noguera JC, Morales J, Pérez C, Velando A (2010) On the oxidative cost of begging: antioxidants enhance vocalizations in gull chicks. Behav Ecol 21:479–484CrossRefGoogle Scholar
  44. Osorno JL, Drummond H (1995) The function of hatching asynchrony in the blue-footed booby. Behav Ecol Sociobiol 37:265–273CrossRefGoogle Scholar
  45. Ostreiher R, Pruett-Jones S, Heifetz A (2012) Asymmetric contests at the nest. Behav Ecol Sociobiol 66:1237–1246CrossRefGoogle Scholar
  46. Parker GA, Royle NJ, Hartley IR (2002) Begging scrambles with unequal chicks: interactions between need and competitive ability. Ecol Lett 5:206–215CrossRefGoogle Scholar
  47. Podlas KA, Richner H (2013) The adaptive function of hatching asynchrony: an experimental study in great tits. Anim Behav 86:567–576CrossRefGoogle Scholar
  48. R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  49. Ricklefs RE (1965) Brood reduction in the curve-billed thrasher. Condor 67:505–510CrossRefGoogle Scholar
  50. Roulin A, Dreiss AN (2012) Sibling competition and cooperation over parental care. In: Royle NJ, Smiseth PT, Kölliker M (eds) The evolution of parental care. Oxford University Press, Oxford, pp 133–149CrossRefGoogle Scholar
  51. Royle NJ, Hamer KC (1998) Hatching asynchrony and sibling size hierarchies in gulls: effects on parental investment decisions, brood reduction and reproductive success. J Avian Biol 29:266–272CrossRefGoogle Scholar
  52. Schwabl H (1997) A hormonal mechanism for parental favouritism. Nature 386:231CrossRefGoogle Scholar
  53. Siegel RB, Weathers WW, Beissinger SR (1999) Hatching asynchrony reduces the duration, not the magnitude, of peak load in breeding green-rumped parrotlets (Forpus passerinus). Behav Ecol Sociobiol 45:444–450CrossRefGoogle Scholar
  54. Smiseth PT, Morgan K (2009) Asynchronous hatching in burying beetles: a test of the peak load reduction hypothesis. Anim Behav 77:519–524CrossRefGoogle Scholar
  55. Stearns S (1992) The evolution of life histories. Oxford University Press, OxfordGoogle Scholar
  56. Stenning MJ (1996) Hatching asynchrony, brood reduction and other rapidly reproducing hypotheses. Trends Ecol Evol 11:243–246PubMedCrossRefGoogle Scholar
  57. Therneau T (2012) coxme: mixed effects Cox models. R package version 2.2-3.
  58. Vallarino A, Evans N, Daunt F, Wanless S, Nager R (2012) Egg components vary independently of each other in the facultative siblicidal black-legged Kittiwake Rissa tridactyla. J Ornithol:1–11Google Scholar
  59. Venables WN, Ripley BD (2002) Modern applied statistics with S. Springer, New YorkCrossRefGoogle Scholar
  60. Viñuela J (1999) Sibling aggression, hatching asynchrony, and nestling mortality in the black kite (Milvus migrans). Behav Ecol Sociobiol 45:33–45CrossRefGoogle Scholar
  61. Viñuela J (2000) Opposing selective pressures on hatching asynchrony: egg viability, brood reduction, and nestling growth. Behav Ecol Sociobiol 48:333–343CrossRefGoogle Scholar
  62. White J, Leclaire S, Kriloff M, Mulard H, Hatch SA, Danchin E (2010) Sustained increase in food supplies reduces broodmate aggression in black-legged kittiwakes. Anim Behav 79:1095–1100CrossRefGoogle Scholar
  63. Wiebe KL, Bortolotti GR (1994a) Food supply and hatching spans of birds: energy constraints or facultative manipulation. Ecology 75:813–823CrossRefGoogle Scholar
  64. Wiebe KL, Bortolotti GR (1994b) Energetic efficiency of reproduction: the benefits of asynchronous hatching for American kestrels. J Anim Ecol:551–560Google Scholar
  65. Wiebe KL, Bortolotti GR (2000) Parental interference in sibling aggression in birds: what should we look for? Ecoscience 7:1–9Google Scholar
  66. Wiehn J, Ilmonen P, Korpimäki E, Pahkala M, Wiebe KL (2000) Hatching asynchrony in the Eurasian kestrel Falco tinnunculus: an experimental test of the brood reduction hypothesis. J Anim Ecol 69:85–95CrossRefGoogle Scholar
  67. Williams GC (1966) Natural selection, the costs of reproduction, and a refinement of Lack's principle. Am Nat 100:687–690CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2013

Authors and Affiliations

  • Thomas Merkling
    • 1
    • 2
    Email author
  • Lena Agdere
    • 1
    • 2
  • Elise Albert
    • 1
    • 2
  • Romain Durieux
    • 1
    • 2
  • Scott A. Hatch
    • 3
    • 4
  • Etienne Danchin
    • 1
    • 2
  • Pierrick Blanchard
    • 1
    • 2
  1. 1.UMR5174 EDB (Laboratoire Évolution & Diversité Biologique), CNRS, ENFAUniversité Toulouse 3 Paul SabatierToulouseFrance
  2. 2.CNRS, UMR5174 EDBUniversité Paul SabatierToulouseFrance
  3. 3.U.S. Geological SurveyAlaska Science CenterAnchorageUSA
  4. 4.Institute for Seabird Research and ConservationAnchorageUSA

Personalised recommendations