Skip to main content
Log in

Testosterone increases siblicidal aggression in black-legged kittiwake chicks (Rissa tridactyla)

  • Original Paper
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

To compete for parental food deliveries nestling birds have evolved diverse behaviors such as begging displays and sibling aggression. Testosterone has been suggested to be an important mechanism orchestrating such competitive behaviors, but evidence is scarce and often indirect. Siblicidal species provide an interesting case in which a clear dominance hierarchy is established and the dominant chicks lethally attack siblings. We experimentally elevated testosterone in chicks of a facultatively siblicidal species, the black-legged kittiwake, Rissa tridactyla, and showed that testosterone-treated chicks were more aggressive toward their sibling than were control chicks. In such facultatively siblicidal species, chicks normally exhibit intense aggression only when threatened by starvation. Indeed, we found that chicks in relatively poorer condition were more aggressive than were chicks in better condition, even among testosterone-treated chicks, suggesting the action of an additional signal modulating aggression. Relatively larger siblings were also more aggressive than were relatively smaller siblings, confirming the importance of size advantage in determining dominance hierarchies within the brood. In addition, testosterone increased aggression toward a simulated predator, indicating that in kittiwakes testosterone can increase aggression in contexts other than siblicide. Testosterone promoted aggression-mediated dominance, which increased begging although testosterone treatment did not have a significant separate effect on begging. Therefore, testosterone production in the kittiwake and most likely other siblicidal species seems an important fitness mediator already early in life, outside the sexual context and not only manifesting itself in aggressive behavior but also in dominance-mediated effects on food solicitation displays toward parents.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Bates D, Maechler M, Bolker B (2011) lme4: linear mixed-effects models using S4 classes. R package version 0.999375-42. http://cran.r-project.org/web/packages/lme4

  • Bookstein FL (1989) “Size and Shape”: a comment on symantics. Syst Zool 38:173–180

    Article  Google Scholar 

  • Braun BM, Hunt GL Jr (1983) Brood reduction in black-legged kittiwakes. Auk 100:469–476

    Google Scholar 

  • Burger J, Gochfeld M (1984) Great black-backed gull predation on kittiwake fledglings in Norway. Bird Study 31:149–151

    Article  Google Scholar 

  • Cullen E (1957) Adaptations in the kittiwake to cliff-nesting. Ibis 88:275–302

    Google Scholar 

  • Development Core Team R (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Drummond H (2001) A revaluation of the role of food in broodmate aggression. Anim Behav 61:517–526

    Article  Google Scholar 

  • Drummond H (2002) Begging versus aggression in avian broodmate competition. In: Wright J, Leonard ML (eds) The evolution of begging: competition, cooperation and communication. Kluwer Academic Publishers, Dordrecht, pp 337–360

    Chapter  Google Scholar 

  • Drummond H (2006) Dominance in vertebrate broods and litters. Q Rev Biol 81:3–31

    Article  PubMed  Google Scholar 

  • Drummond H, Garcia Chavelas C (1989) Food shortage influences sibling aggression in the blue-footed booby. Anim Behav 37:806–819

    Article  Google Scholar 

  • Dunn EH (1980) On the variability in energy allocation of nestling birds. Auk 97:19v27

    Google Scholar 

  • Ferree ED, Wikelski MC, Anderson DJ (2004) Hormonal correlates of siblicide in Nazca boobies: support for the Challenge Hypothesis. Horm Behav 46:655–662

    Article  CAS  PubMed  Google Scholar 

  • Forbes LS (2007) Sibling symbiosis in nestling birds. Auk 124:1–10

    Article  Google Scholar 

  • Glassey B, Forbes LS (2002) Begging and asymmetric nestling competition. In: Wright J, Leonard ML (eds) The evolution of begging: competition, cooperation and communication. Kluwer Academic Publishers, Dordrecht, pp 269–281

    Chapter  Google Scholar 

  • Goodship NM, Buchanen KL (2007) Nestling testosterone controls begging behaviour in the pied flycatcher, Ficedula hypoleuca. Horm Behav 52:454–460

    Article  CAS  PubMed  Google Scholar 

  • Groothuis T, Meeuwissen G (1992) The influence of testosterone on the development and fixation of the form of displays in two age classes of young black-headed gulls. Anim Behav 43:189–208

    Article  Google Scholar 

  • Groothuis TGG, Ros AFH (2005) The hormonal control of begging and early aggressive behavior: experiments in black-headed gulls. Horm Behav 48:207–215

    Article  CAS  PubMed  Google Scholar 

  • Hatch SA, Robertson GJ, Baird PH (2009) Black-legged Kittiwake (Rissa tridactyla). In: Poole A (ed) The birds of North America online. Cornell Lab of Ornithology, Ithaca

    Google Scholar 

  • Helfenstein F, Tirard C, Danchin E, Wagner RH (2004) Low frequency of extra-pair paternity and high frequency of adoption in black-legged kittiwakes. Condor 106:149–155

    Article  Google Scholar 

  • Ibáñez-Álamo JD, Chastel O, Soler M (2011) Hormonal response of nestlings to predator calls. Gen Comp Endocrinol 171:232–236

    Article  PubMed  Google Scholar 

  • Irons DB (1992) Aspect of foraging behavior and reproductive biology of the blacklegged kittiwake. PhD thesis, University of California, Irvine

  • Jacobsen KO, Erikstad KE, Saether BE (1995) An experimental study of the costs of reproduction in the kittiwake Rissa tridactyla. Ecology 76:1636–1642

    Article  Google Scholar 

  • Kilner RM (2002) The evolution of complex begging displays. In: Wright J, Leonard ML (eds) The evolution of begging: competition, cooperation and communication. Kluwer Academic Publishers, Dordrecht, pp 87–106

    Chapter  Google Scholar 

  • Kitaysky AS, Piatt JF, Wingfield JC, Romano M (1999) The adrenocortical stress-response of black-legged kittiwake chicks in relation to dietary restrictions. J Comp Physiol B 169:303–310

    Article  CAS  Google Scholar 

  • Kitaysky AS, Wingfield JC, Piatt JG (2001) Corticosterone facilitates begging and affects resource allocation in the black-legged kittiwake. Behav Ecol 12:619–625

    Article  Google Scholar 

  • Kitaysky AS, Kitaiskaia EV, Piatt JF, Wingfield JC (2003) Benefits and costs of increased levels of corticosterone in seabird chicks. Horm Behav 43:140–149

    Article  CAS  PubMed  Google Scholar 

  • Lee KA (2006) Linking immune defenses and life history at the levels of the individual and the species. Integr Comp Biol 46:1000–1015

    Article  CAS  PubMed  Google Scholar 

  • Lessells CM (2008) Neuroendocrine control of life histories: what do we need to know to understand the evolution of phenotypic plasticity? Philos Trans R Soc B 363:1589–1598

    Article  Google Scholar 

  • MacCarone AD (1992) Predation by common ravens on cliff-nesting black-legged kittiwakes on Baccalieu Island, Newfoundland. Col Waterbirds 15:253–256

    Article  Google Scholar 

  • Maindonald J, Braun WJ (2003) Data analysis and graphics using R – an example-based approach. Cambridge University Press, UK

    Google Scholar 

  • Mathevon N, Charrier I (2004) Parent–offspring conflict and the coordination of siblings in gulls. Proc R Soc Lond B 271:S145–S147

    Article  Google Scholar 

  • Müller MS, Brennecke JF, Porter ET, Ottinger MA, Anderson DJ (2008) Perinatal androgens and adult behavior vary with nestling social system in siblicidal boobies. PLoS ONE 3:e2460

    Article  PubMed Central  PubMed  Google Scholar 

  • Müller MS, Roelofs Y, Erikstad KE, Groothuis TGG (2012) Maternal androgens increase sibling aggression, dominance, and competitive ability in the siblicidal black-legged kittiwake (Rissa tridactyla). PLoS ONE 7:e47763

    Article  PubMed Central  PubMed  Google Scholar 

  • Nuñez-de la Mora A, Drummond H, Wingfield JC (1996) Hormonal correlates of dominance and starvation-induced aggression in chicks of the blue-footed booby. Ethology 102:748–761

    Article  Google Scholar 

  • Pierotti R, Murphy EC (1987) Intergenerational conflicts in gulls. Anim Behav 35:435–444

    Article  Google Scholar 

  • Price K, Harvey H, Ydenberg R (1996) Begging tactics of nestling yellow-headed blackbirds, Xanthocephalus xanthocephalus, in relation to need. Anim Behav 51:421–435

    Article  Google Scholar 

  • Ramos-Fernandez G, Nuñez-de la Mora A, Wingfield JC, Drummond H (2000) Endocrine correlates of dominance in chicks of the blue-footed booby (Sula nebouxii): testing the Challenge Hypothesis. Ethol Ecol Evol 12:27–34

    Article  Google Scholar 

  • Roberts BD, Hatch SA (1994) Chick movements and adoption in a colony of black-legged kittiwakes. Wilson Bull 106:289–298

    Google Scholar 

  • Ros AFH (1997) Role of sensitization to testosterone in the early development of aggression in the black-headed gull. Unpublished doctoral dissertation, University of Groningen, Netherlands

  • Ros AFH (2008) Patterns of testosterone responsiveness and immunity in relation to competitive behavior in chicks. Horm Behav 54:234–237

    Article  CAS  PubMed  Google Scholar 

  • Ros AFH, Groothuis TGG, Apanius V (1997) The relation among gonadal steroids, immunocompetence, body mass, and behavior in young black-headed gulls (Larus ridibundus). Am Nat 150:201–219

    Article  CAS  PubMed  Google Scholar 

  • Ros AFH, Dieleman SJ, Groothuis TGG (2002) Social stimuli, testosterone, and aggression in gull chicks: support for the challenge hypothesis. Horm Behav 41:334–342

    Article  CAS  PubMed  Google Scholar 

  • Roulin A (2002) The sibling negotiation hypothesis. In: Wright J, Leonard ML (eds) The evolution of begging: competition, cooperation and communication. Kluwer Academic Publishers, Dordrecht, pp 107–126

    Chapter  Google Scholar 

  • Saino N, Møller AP (2002) Immunity and begging. In: Wright J, Leonard ML (eds) The evolution of begging: competition, cooperation and communication. Kluwer Academic Publishers, Dordrecht, pp 245–267

  • Sasvari L, Hegyi Z, Peczely P (1999) Brood reduction in white storks mediated through asymmetries in plasma testosterone concentrations in chicks. Ethology 105:569–582

    Article  Google Scholar 

  • Smiseth PT, Pellissier Scott M, Andrews C (2011) Hormonal regulation of offspring begging and mediation of parent–offspring conflict. Anim Behav 81:507–517

    Article  Google Scholar 

  • Storey AE, Anderson RE, Porter JM, MacCharles AM (1992) Absence of parent–young recognition in kittiwakes: a re-examination. Behaviour 120:302–323

    Article  Google Scholar 

  • Tarlow EM, Wikelski M, Anderson DJ (2001) Hormonal correlates of siblicide in Galapagos Nazca boobies. Horm Behav 40:14–20

    Article  CAS  PubMed  Google Scholar 

  • 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 79:1095–1100

    Article  Google Scholar 

Download references

Acknowledgments

We gratefully thank Bonnie de Vries and Ilse Weites for help with testosterone assays and Roald Hansen for extensive logistical support in Ekkeroy. We thank Kjell Einar Erikstad for integrating our work in the study colony with the ongoing seabird monitoring (SEAPOP), and we thank the County Governor of Finnmark for permission. We thank the associate editor Marty Leonard and two anonymous referees for helpful suggestions.

Ethical standards

This experiment complied with the laws of Norway and the research permit issued by the Norwegian Animal Research Authority.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Martina S. Müller.

Additional information

Communicated by M. Leonard

Rights and permissions

Reprints and permissions

About this article

Cite this article

Müller, M.S., Moe, B. & Groothuis, T.G.G. Testosterone increases siblicidal aggression in black-legged kittiwake chicks (Rissa tridactyla). Behav Ecol Sociobiol 68, 223–232 (2014). https://doi.org/10.1007/s00265-013-1637-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-013-1637-z

Keywords

Navigation