Skip to main content
SpringerLink
Log in

Different recognition cues reveal the decision rules used for egg rejection by hosts of a variably mimetic avian brood parasite

  • Original Paper
  • Published:
Animal Cognition Aims and scope Submit manuscript

Abstract

Brood parasitism imposes several fitness costs on the host species. To reduce these costs, hosts of avian brood parasites have evolved various defenses, of which egg rejection is the most prevalent. In the face of variable host-parasite mimicry and the costs of egg discrimination itself, many hosts reject only some foreign eggs. Here, we experimentally varied the recognition cues to study the underlying cognitive mechanisms used by the Chalk-browed Mockingbird (Mimus saturninus) to reject the white immaculate eggs laid by the parasitic Shiny Cowbird (Molothrus bonariensis). Immaculate eggs are the only parasite eggs rejected by this host, as it accepts all polymorphic, spotted eggs laid by cowbirds. Using a within-breeding pair experimental design, we tested for the salience of spotting, UV reflectance, and brightness in eliciting rejection. We found that the presence of spotting significantly decreased the probability of rejection while increments in brightness significantly increased rejection frequencies. The cognitive rules underlying mockingbird rejection behavior can be explained by a decision-making model which predicts changes in the levels of rejection in direct relation to the number of relevant attributes shared between host and parasite eggs.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Antonov A, Stokke BG, Moksnes A, Røskaft E (2009) Evidence for egg discrimination preceding failed rejection attempts in a small cuckoo host. Biol Lett 5:166–171

    Google Scholar 

  • Avilés JM, Rutila J, Moller AP (2005) Should the redstart (Phoenicurus phoenicurus) accept or reject cuckoo eggs? Behav Ecol Sociobiol 58:608–617

    Article  Google Scholar 

  • Avilés JM, Soler JJ, Pérez-Contreras T (2006) Dark nests and egg colour in birds: a possible functional role of ultraviolet reflectance in egg detectability. Proc R Soc Lond B 273:2821–2829

    Article  Google Scholar 

  • Avilés JM, Vikan J, Fossøy F, Antonov A, Mosknes A, Røskaft E, Stokke BG (2010) Avian colour perception predicts behavioural responses to experimental brood parasitism in chaffinches. J Evol Biol 23:293–301

    Article  PubMed  Google Scholar 

  • Bowmaker JK, Heath LA, Wilkie SE, Hunt DM (1997) Visual pigments and oil droplets from six classes of photoreceptor in the retinas of birds. Vision Res 37:2183–2194

    Article  PubMed  CAS  Google Scholar 

  • Cassey P, Honza M, Grim T, Hauber ME (2008) The modelling of avian visual perception predicts behavioural rejection responses to foreign egg colours. Biol Lett 4:515–517

    Article  PubMed  Google Scholar 

  • Davies NB (2000) Cuckoos, cowbirds and other cheats. T and AD Poyser, London

    Google Scholar 

  • Davies NB (2011) Cuckoo adaptations: trickery and tuning. J Zool 284:1–14

    Article  Google Scholar 

  • de la Colina MA, Mahler B, Reboreda JC (2011) Differences in morphology and colour pattern of shiny cowbird (Molothrus bonariensis) eggs found in nests of two hosts. Biol J Linn Soc 102:838–845

    Article  Google Scholar 

  • De Mársico MC, Mahler B, Chomnalez M, Di Giacomo AG, Reboreda JC (2010) Host use by generalist and specialist brood parasitic cowbirds at population and individual levels. Adv Study Behav 42:83–121

    Article  Google Scholar 

  • Fiorini VD, Reboreda JC (2006) Cues used by shiny cowbirds (Molothrus bonariensis) to locate and parasitise chalk-browed mockingbird (Mimus saturninus) nests. Behav Ecol Sociobiol 60:379–385

    Article  Google Scholar 

  • Fiorini VD, Tuero DT, Reboreda JC (2009) Host behaviour and nest-site characteristics affect the likelihood of brood parasitism by shiny cowbirds on chalk-browed mockingbirds. Behav 146:1387–1403

    Article  Google Scholar 

  • Fraga RM (1985) Host–parasite interactions between chalk-browed mockingbirds and shiny cowbirds. Ornithol Monog 36:829–844

    Google Scholar 

  • Friedmann H (1929) The cowbirds: a study in the biology of social parasitism. C.C.Thomas, Springfield

    Google Scholar 

  • Gloag R, Fiorini VD, Reboreda JC, Kacelnik A (2012) Brood parasite eggs enhance egg survivorship in a multiply parasitized host. Proc R Soc Lond B 279:1831–1839

    Article  Google Scholar 

  • Grim T (2007) Experimental evidence for chick discrimination without recognition in a brood parasite host. Proc R Soc Lond B 274:373–381

    Article  Google Scholar 

  • Grim T, Samaš P, Moskát C, Kleven O, Honza M, Moksnes A, Røskaft E, Stokke BG (2011) Constraints on host choice: why do parasitic birds rarely exploit some common potential hosts? J Anim Ecol 80:508–518

    Article  PubMed  Google Scholar 

  • Gross MR (1996) Alternative reproductive strategies and tactics: diversity within sexes. Trends Ecol Evol 11:92–98

    Article  PubMed  CAS  Google Scholar 

  • Hauber ME (2002) Is reduced clutch size a cost of parental care in Eastern Phoebes (Sayornis phoebe)? Behav Ecol Sociobiol 51:503–509

    Article  Google Scholar 

  • Hauber ME (2003) Hatching asynchrony, nestling competition, and the cost of interspecific brood parasitism. Behav Ecol 14:224–235

    Article  Google Scholar 

  • Hauber ME, Moskát C, Bán M (2006) Experimental shift in hosts’ acceptance threshold of inaccurate-mimic brood parasite eggs. Biol Lett 2:177–180

    Article  PubMed  Google Scholar 

  • Holen ØH, Johnstone RA (2004) The evolution of mimicry under constraints. Am Nat 164:598–613

    Article  PubMed  Google Scholar 

  • Honza M, Polačiková L (2008) Experimental reduction of ultraviolet wavelength reflected from parasitic eggs affects rejection behaviour in the blackcap Sylvia atricapilla. J Exp Biol 211:2519–2523

    Article  PubMed  Google Scholar 

  • Honza M, Polačiková L, Prochazka P (2007) Ultraviolet and green parts of the colour spectrum affect egg rejection in the song thrush (Turdus philomelos). Biol J Linn Soc 92:269–276

    Article  Google Scholar 

  • Honza M, Procházka P, Morongová K, Čapek M, Jelínek V (2011) Do nest light conditions affect rejection of parasitic eggs? A test of the light environment hypothesis. Ethology 117:539–546

    Article  Google Scholar 

  • Hoover JP (2003) Multiple effects of brood parasitism reduce the reproductive success of prothonotary warblers, Protonotaria citrea. Anim Behav 65:923934

    Google Scholar 

  • Hudson WH (1874) Notes on the procreant instincts of the three species of Molothrus found in Buenos Aires. Proc Zool Soc 11:153–174

    Google Scholar 

  • Igic B, Cassey P, Grim T, Greenwood DR, Moskát C, Rutila J, Hauber ME (2011) A shared chemical basis of avian host–parasite egg colour mimicry. Proc R Soc B. doi:10.1098/rspb.2011.1718

    PubMed  Google Scholar 

  • Kilner RM, Langmore NE (2011) Cuckoos versus hosts in insects and birds: adaptations, counter-adaptations and outcomes. Biol Rev 86:836–852

    Article  PubMed  Google Scholar 

  • Lahti DC (2006) Persistence of egg recognition in the absence of cuckoo brood parasitism: pattern and mechanism. Evolution 60:157–168

    PubMed  Google Scholar 

  • Lahti DC, Lahti AR (2002) How precise is egg discrimination in weaverbirds? Anim Behav 63:1135–1142

    Article  Google Scholar 

  • Langmore NE, Hunt S, Kilner RM (2003) Escalation of a coevolutionary arms race through host rejection of brood parasitic young. Nature 422:157–160

    Article  PubMed  CAS  Google Scholar 

  • Langmore NE, Kilner RM, Butchart SHM, Maurer G, Davies NB, Cockburn A, Macgregor NA, Peters A, Magrath MJL, Dowling DK (2005) The evolution of egg rejection by cuckoo hosts in Australia and Europe. Behav Ecol 16(4):686–692

    Article  Google Scholar 

  • Lindholm AK (2000) Tests of phenotypic plasticity in reed warbler defences against cuckoo parasitism. Behav 137:43–60

    Article  Google Scholar 

  • López-de-Hierro MDG, Moreno-Rueda G (2010) Egg-spot pattern rather than egg colour affects conspecific egg rejection in the house sparrow (Passer domesticus). Behav Ecol Sociobiol 64:317–324

    Article  Google Scholar 

  • Lotem A (1993) Learning to recognize nestlings is maladaptive for cuckoo Cuculus canorus host. Nature 362:743–745

    Article  Google Scholar 

  • Lowther PE (2011) Lists of victims and hosts of the parasitic Cowbirds, Version 03 March 2011. The Field Museum, Chicago. http://fm1.fieldmuseum.org/aa/Files/lowther/CBList.pdf

  • Mahler B, Confalonieri VA, Lovette IJ, Reboreda JC (2008) Eggshell spotting in brood parasitic shiny cowbirds (Molothrus bonariensis) is not linked to the female sex chromosome. Behav Ecol Sociobiol 62:1193–1199

    Article  Google Scholar 

  • Marchetti K (2000) Egg rejection in a passerine bird: size does matter. Anim Behav 59:877–885

    Article  PubMed  Google Scholar 

  • Mason P (1986) Brood parasitism in a host generalist, the shiny cowbird: I. The quality of different species as hosts. Auk 103:52–60

    Google Scholar 

  • McLean IG, Maloney RF (1998) Brood parasitism, recognition, and response: the options. In: Rothstein SI, Robinson SK (eds) Parasitic birds and their hosts, studies in coevolution. Oxford University Press, New York, pp 255–269

    Google Scholar 

  • Moksnes A, Røskaft E, Braa AT (1991) Rejection behaviour by common cuckoo hosts towards artificial brood parasite eggs. Auk 108:348–354

    Google Scholar 

  • Moskát C, Hauber ME (2007) Conflict between egg recognition and egg rejection decisions in common cuckoo (Cuculus canorus) hosts. Anim Cogn 10:377–386

    Article  PubMed  Google Scholar 

  • Moskát C, Szekely T, Cuthill IC, Kisbenedek T (2008) Hosts’ responses to parasitic eggs: which cues elicit hosts’ egg discrimination? Ethology 114:186–194

    Article  Google Scholar 

  • Moskát C, Bán M, Székely T, Komdeur J, Lucassen RWG, van Boheemen AL, Hauber ME (2010) Discordancy or template-based recognition? Dissecting the cognitive basis of the rejection of foreign eggs in hosts of avian brood parasites. J Exp Biol 213:1976–1983

    Article  PubMed  Google Scholar 

  • Nolan JV, Thompson CF (1978) Egg volume as a predictor of hatchling weight in the brown-headed cowbird (Molothrus ater). Wilson Bull 90:353–355

    Google Scholar 

  • Øien IJ, Moksnes A, Røskaft E, Honza M (1998) Costs of Cuckoo Cuculus canorus parasitism to Reed Warblers Acrocephalus scirpaceus. J Avian Biol 29:209–215

    Article  Google Scholar 

  • Osorio D, Ham AD (2002) Spectral reflectance and directional properties of structural coloration in bird plumage. J Exp Biol 205:2017–2027

    PubMed  CAS  Google Scholar 

  • Payne RB, Payne LL (1998) Nestling eviction and vocal begging behaviors in Australian glossy cuckoos Chrysococcyx basalis and C. lucidus. In: Rothstein SI, Robinson SK (eds) Parasitic birds and their hosts, studies in coevolution. Oxford University Press, New York, pp 152–169

    Google Scholar 

  • Peer BD, Sealy SG (2004) Correlates of egg rejection in hosts of the brown-headed cowbird. Condor 106:580–599

    Article  Google Scholar 

  • Polačiková L, Grim T (2010) Blunt egg pole holds cues for alien egg discrimination: experimental evidence. J Avian Biol 41:111–116

    Article  Google Scholar 

  • Polačiková L, Hauber ME, Prochazka P, Cassey P, Honza M, Grim T (2011) A sum of its parts? Relative contributions of different eggshell regions to intraclutch variation in birds. J Avian Biol 42:370–373

    Article  Google Scholar 

  • Pompilio L, Kacelnik A (2010) Context dependent utility overrides absolute memory as a determinant of choice. PNAS 107:508–512

    Article  PubMed  CAS  Google Scholar 

  • Reboreda JC, Mermoz ME, Massoni V, Astié AA, Rabuffetti FL (2003) Impacto del parasitismo de cría del Tordo Renegrido (Molothrus bonariensis) sobre el éxito reproductivo de sus hospedadores. Hornero 18:7788

    Google Scholar 

  • Reeve H (1989) The evolution of conspecific acceptance thresholds. Am Nat 133:407435

    Article  Google Scholar 

  • Røskaft E, Moksnes A, Stokke BG, Moskát C, Honza M (2002a) The spatial habitat structure of host populations explains the pattern of rejection behaviour in hosts and parasitic adaptations in cuckoos. Behav Ecol 13:163168

    Article  Google Scholar 

  • Røskaft E, Moksnes A, Meilvang D, Bicık V, Jemelıkova J, Honza M (2002b) No evidence for recognition errors in Acrocephalus warblers. J Avian Biol 33:31–38

    Article  Google Scholar 

  • Rothstein SI (1974) Mechanisms of avian egg recognition: possible learned and innate factors. Auk 91:796–807

    Google Scholar 

  • Rothstein SI (1982) Mechanisms of avian egg recognition: which egg parameters elicit responses by rejecter species? Behav Ecol Sociobiol 11:229–239

    Article  Google Scholar 

  • Rothstein SI (1990) A model system for coevolution: avian brood parasitism. Annu Rev Ecol Syst 21:481–508

    Article  Google Scholar 

  • Rothstein SI, Robinson SK (1998) Major unanswered questions in the study of avian brood parasitism. In: Rothstein SI, Robinson SK (eds) Parasitic birds and their hosts, studies in coevolution. Oxford University Press, New York, pp 419–425

    Google Scholar 

  • Sackmann P, Reboreda JC (2003) A comparative study of shiny cowbird parasitism in two large hosts: chalk-browed mockingbird and rufous-belied thrush. Condor 105:728–736

    Article  Google Scholar 

  • Safran RJ, Vitousek MN (2008) Evolutionary biology: arms races in the eye of the beholder. Curr Biol 18:734–736

    Article  Google Scholar 

  • Samaš P, Hauber ME, Cassey P, Grim T (2011) Repeatability of foreign egg rejection: testing the assumptions of co-evolutionary theory. Ethology 117:606–619

    Article  Google Scholar 

  • Schuetz JG (2005) Reduced growth but not survival of chicks with altered gape patterns: implications for the evolution of nestling similarity in a parasitic finch. Anim Behav 70:839–848

    Article  Google Scholar 

  • Schulze-Hagen K, Stokke BG, Birkhead TR (2009) Reproductive biology of the European cuckoo Cuculus canorus: early insights, persistent errors and the acquisition of knowledge. J Ornithol 150:1–16

    Article  Google Scholar 

  • Servedio M, Hauber ME (2006) To eject or to abandon? Brood parasite virulence and host clutch sizes interact to influence the fitness payoffs of alternative rejection strategies. J Evol Biol 19:1585–1594

    Article  PubMed  CAS  Google Scholar 

  • Servedio MR, Lande R (2003) Coevolution of an avian host and its parasitic cuckoo. Evolution 57:1164–1175

    PubMed  Google Scholar 

  • Spottiswoode C, Stevens M (2010) Visual modeling shows that avian host parents use multiple visual cues in rejecting parasitic eggs. PNAS 19:8672–8676

    Article  Google Scholar 

  • Stoddard MC, Stevens M (2010) Pattern mimicry of host eggs by the common cuckoo, as seen through a bird’s eye. Proc R Soc B 277:1387–1393

    Article  PubMed  Google Scholar 

  • Stoddard MC, Stevens M (2011) Avian vision and the evolution of egg color mimicry in the common cuckoo. Evolution 65:2004–2013

    Article  PubMed  Google Scholar 

  • Stokke BG, Moksnes A, Røskaft E (2005) The enigma of imperfect adaptations in hosts of avian brood parasites. Ornithol Sci 4:17–29

    Article  Google Scholar 

  • Tokue K, Ueda K (2010) Mangrove Gerygones Gerygone laevigaster eject Little Bronze-cuckoo Chalcites minutillus hatchlings from parasitized nests. Ibis 152:835–839

    Article  Google Scholar 

  • Tuero DT, Fiorini VD, Reboreda JC (2007) Effects of shiny cowbird parasitism on different components of house wren reproductive success. Ibis 149:521–529

    Article  Google Scholar 

  • Underwood TJ, Sealy SG (2006) Parameters of brown-headed cowbird Molothrus ater egg discrimination in warbling vireos Vireo gilvus. J Avian Biol 37:457–466

    Article  Google Scholar 

  • Vikan JR, Stokke BG, Fossøy F, Jackson C, Huhta E, Rutila J, Moksnes A, Røskaft E (2009) Fixed rejection responses to single and multiple experimental parasitism in two Fringilla hosts of the common cuckoo. Ethology 115:840–850

    Article  Google Scholar 

  • Wedell DH (1991) Distinguishing among models of contextually induced preference reversals. J Exp Psych Learn Mem Cogn 17:767–778

    Article  Google Scholar 

Download references

Acknowledgments

We thank Fundación Elsa Shaw de Pearson for allowing us to conduct this study at the “Reserva El Destino.” We also thank Martín Rossi for statistical support and Tomas Grim for his help in various aspects of this study. MAdlC was supported by a fellowship of the Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT). BM, LP, and JCR are research fellows of the Consejo Nacional de Investigaciones Científicas y Técnicas. We thank the New Zealand Royal Society (ISAT), the PSC-CUNY grant funds, and the Human Frontier Science Program for additional funding to BM and MEH. This work was supported by grants from ANPCyT and Universidad de Buenos Aires.

Author information

Authors and Affiliations

  1. Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Pabellón II Ciudad Universitaria, C1428EGA, Buenos Aires, Argentina

    M. Alicia de la Colina, Lorena Pompilio, Juan C. Reboreda & Bettina Mahler

  2. Department of Psychology, Hunter College and the Graduate Center, City University of New York, New York, NY, 10065, USA

    Mark E. Hauber

Authors
  1. M. Alicia de la Colina
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lorena Pompilio
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Mark E. Hauber
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Juan C. Reboreda
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bettina Mahler
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to M. Alicia de la Colina.

Rights and permissions

Reprints and permissions

About this article

Cite this article

de la Colina, M.A., Pompilio, L., Hauber, M.E. et al. Different recognition cues reveal the decision rules used for egg rejection by hosts of a variably mimetic avian brood parasite. Anim Cogn 15, 881–889 (2012). https://doi.org/10.1007/s10071-012-0515-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10071-012-0515-9

Keywords

Search

Navigation