Skip to main content
SpringerLink
Log in

Spectral tuning and perceptual differences do not explain the rejection of brood parasitic eggs by American robins (Turdus migratorius)

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

Abstract

By laying their eggs in the nests of other birds, avian brood parasites impose the cost of rearing young upon their hosts. The recognition and rejection of foreign eggs are primary host defenses against costly brood parasitism. Hosts of parasitic brown-headed cowbirds (Molothrus ater) challenge coevolutionary theory because most cowbird hosts accept parasitic eggs despite their drastically different appearance from the hosts’ own eggs. American robins (Turdus migratorius) are one of only 10 % of the over 200 potential cowbird host species to robustly reject parasitic eggs, but the mechanisms driving the sensory bases of foreign egg rejection remain elusive. Our research combined avian visual perceptual modeling and behavioral experimentation to investigate chromatic cues eliciting parasitic egg rejection in American robins. We assessed the effects of perceivable background color differences between real host and model parasite eggs, across all four avian photoreceptors, on rates of rejection of model eggs spanning in color across the entire avian spectral sensitivity range, and including immaculate model eggs matching the natural colors of robin and cowbird eggs. The results suggest that egg rejection in robins is driven by the overall perceivable difference in color between own and artificial eggs, and input from all four single-cone avian photoreceptors affects the rejection decision. The results, however, also reveal that when viewed by the avian eye, natural cowbird eggs appear more similar in background color to robin eggs than predicted by the high rejection rate of these parasitic eggs. This suggests that robins respond specifically to parasitism by cowbirds, despite an apparent lack of sensory tuning toward the detection of the background color of cowbird 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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aidala Z, Huynen L, Brennan P, Musser J, Fidler A, Chong N, Machovsky Capuska G, Anderson M, Talaba A, Lambert D, Hauber ME (2012a) Ultraviolet visual sensitivity in three avian lineages; paleognaths, parrots, and passerines. J Comp Physiol A 198:495–510

    Article  Google Scholar 

  • Aidala Z, Chong N, Anderson MG, Hauber ME (2012b) Predicted visual sensitivity for short-wavelength light in the brood parasitic cuckoos of New Zealand. Chinese Birds 3:295–301

    Article  Google Scholar 

  • Anderson MG, Ross HA, Brunton DH, Hauber ME (2009) Begging call matching between a specialist brood parasite and its host: a comparative approach to detect coevolution. Biol J Linn Soc 98:208–216

    Article  Google Scholar 

  • Antonov A, Stokke BG, Moksnes A, Røskaft E (2009) Evidence for egg discrimination preceding failed rejection attempts in a small cuckoo host. Biol Lett 5:169–171

    Article  PubMed Central  PubMed  Google Scholar 

  • Avilés JM (2008) Egg color mimicry in the common cuckoo Cuculus canorus as revealed by modelling host retinal function. Proc R Soc Lond B275:2345–2352

    Article  Google Scholar 

  • Avilés JM, Soler JJ, Perez-Contreras T, Soler M, Møller AP (2005) Ultraviolet reflectance of great spotted cuckoo eggs and egg discrimination by magpies. Behav Ecol 17:310–314

    Article  Google Scholar 

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

    Google Scholar 

  • Ban M, Moskát C, Barta Z, Hauber ME (2013) Simultaneous viewing of own and parasitic eggs is not required for egg rejection by a cuckoo host. Behav Ecol 24:1014–1021

    Google Scholar 

  • Bennett ATD, Théry M (2007) Avian color vision and coloration: Multidisciplinary evolutionary biology. The American Naturalist 169:S1–S6

    Google Scholar 

  • Briskie JV, Sealy SG, Hobson KA (1992) Behavioral defenses against avian brood parasitism in sympatric and allopatric host populations. Evolution 46:334–340

    Article  Google Scholar 

  • Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information–theoretic approach. Springer, New York

    Google Scholar 

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

    Article  PubMed Central  PubMed  Google Scholar 

  • Chen D-M, Goldsmith TH (1986) Four spectral classes of cone in the retinas of birds. J Comp Physiol A 159:473–479

    Article  CAS  PubMed  Google Scholar 

  • Chen D-M, Collins JS, Goldsmith TH (1984) The ultraviolet receptor of bird retinas. Science 225:337–340

    Article  CAS  PubMed  Google Scholar 

  • Cherry MI, Bennett ATD (2001) Egg color matching in an African cuckoo, as revealed by ultraviolet-visible reflectance spectrophotometry. Proc R Soc Lond B 268:565–571

    Article  CAS  Google Scholar 

  • Cherry MI, Bennett ATD, Moskat C (2007a) Host intra-clutch variation, cuckoo egg matching and egg rejection by great reed warblers. Naturwissenschaften 94:441–447

    Article  CAS  PubMed  Google Scholar 

  • Cherry MI, Bennett ATD, Moskat C (2007b) Do cuckoos choose nests of great reed warblers on the basis of host egg appearance? J Evol Biol 20:1218–1222

    Article  CAS  PubMed  Google Scholar 

  • Croston R, Hauber ME (2010) The Ecology of Avian Brood Parasitism. Nat Educ Knowledge 1:3

    Google Scholar 

  • Cuthill IC, Partridge JC, Bennett ATD, Church SC, Hart NS, Hunt S (2000) Ultraviolet vision in birds. Adv Study Behav 29:159–213

    Article  Google Scholar 

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

    Google Scholar 

  • Davies NB, Brooke MDL (1988) Cuckoos versus reed warblers: adaptations and counteradaptations. Anim Behav 36:262–284

    Article  Google Scholar 

  • Davies NB, Brooke MDL (1989) An experimental study of co-evolution between the cuckoo, Cuculus canorus, and its hosts. I. Host egg discrimination. J Anim Ecol 58:207–224

    Article  Google Scholar 

  • de la Colina MA, Pompillo L, Hauber ME, Reboreda JC, Mahler B (2012) 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

    Article  PubMed  Google Scholar 

  • Endler JA (1990) On the measurement and classification of color in studies of animal color patterns. Biol J Linn Soc 41:315–352

    Article  Google Scholar 

  • Endler JA, Mielke PW (2005) Comparing entire color patterns as birds see them. Biol J Linn Soc 86:405–431

    Article  Google Scholar 

  • Fernández-Juricic E, Ojeda A, Deisher M, Burry B, Baumhardt P, Stark A, Elmore AG, Ensminger AL (2013) Do male and female cowbirds see their world differently? Implications for sex differences in the sensory system of an avian brood parasite. PLOS One 8:e58985

    Google Scholar 

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

    Google Scholar 

  • Friedmann H (1971) Further information of the host relations of the parasitic cowbirds. Auk 88:239–255

    Article  Google Scholar 

  • Gomez D (2010) AVICOL v.5, a program to analyse spectrometric data. Available from the author at dodogomez@yahoo.fr or by download from http://sites.google.com/site/avicolprogram/

  • Grim T (2006) Cuckoo growth performance in parasitized and unused hosts: not only host size matters. Behav Ecol Sociobiol 60:716–723

    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

    Google Scholar 

  • Guigueno MF, Sealy SG (2012) Increased investigation of manipulated clutches suggests egg recognition without rejection in a Brown-headed Cowbird (Molothrus ater) host, the Yellow Warbler (Setophaga petechia). Auk 129:17–25

    Google Scholar 

  • Hart NS, Partridge JC, Cuthill IC, Bennett ATD (2000) Visual pigments, oil droplets, ocular media and cone photoreceptor distribution in two species of passerine bird: the blue tit (Parus caeruleus L.) and the blackbird (Turdus merula L.). J Comp Physiol A 186:375–387

    Article  CAS  PubMed  Google Scholar 

  • Hauber ME (2003a) Interspecific brood parasitism and the evolution of host clutch sizes. Evol Ecol Res 5:559–570

    Google Scholar 

  • Hauber ME (2003b) Hatching asynchrony, nestling competition, and the cost of interspecific brood parasitism. Behav Ecol 14:227–235

    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

    Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Honza M, Kuiper SM, Cherry MI (2005) Behavior of African turdid hosts towards experimental parasitism with artificial red-chested cuckoo Cuculus solitarius eggs. J Avian Biol 6:517–522

    Article  Google Scholar 

  • Honza M, Polačiková L, Procházka P (2007) Ultraviolet and green parts of the color 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 

  • Hosoi S, Rothstein S (2000) Nest desertion and cowbird parasitism: evidence for evolved responses and evolutionary lag. Anim Behav 59:823–840

    Article  PubMed  Google Scholar 

  • Igic B, Leuschner N, Parker KA, Ismar SMH, Gill BJ, Lovegrove TG, Millar CD, Hauber ME (2010) Size dimorphism and avian-perceived sexual dichromatism in a New Zealand endemic bird, the whitehead Mohoua albicilla. J Morphol 271:697–704

    PubMed  Google Scholar 

  • Igic B, Cassey P, Grim T, Greenwood DR, Moskát C, Rutila J, Hauber ME (2012) A shared chemical basis of avian host–parasite egg color mimicry. Proc R Soc Lond B 279:1068–1076

    Article  Google Scholar 

  • Kilner RM (2003) How selfish is a cowbird nestling? Anim Behav 66:569–576

    Article  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 

  • Kilner RM, Madden JR, Hauber ME (2004) Nestlings use host young to procure resources. Science 305:877–879

    Article  CAS  PubMed  Google Scholar 

  • Kilpatrick AM (2002) Variation in growth of brown-headed cowbird (Molothrus ater) nestlings and energetic impacts on their host parents. Can J Zool 80:145–153

    Article  Google Scholar 

  • Klippenstine DR, Sealy SG (2010) Assessing generalized egg mimicry: a quantitative comparison of eggs of brown-headed cowbirds and grassland passerines. Wilson J Ornithol 122:346–353

    Article  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, 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 16:686–692

    Article  Google Scholar 

  • Langmore NE, Stevens M, Maurer G, Kilner RM (2009) Are dark cuckoo eggs cryptic in host nests? Anim Behav 78:461–468

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Lorenzana JC, Sealy SG (2001) Fitness costs and benefits of cowbird egg ejection by gray catbirds. Behav Ecol 12:325–329

    Article  Google Scholar 

  • Lowther PE (1993) Brown-headed cowbird (Molothrus ater). In: Poole (ed) The Birds of North America Online. Cornell Lab of Ornithology, Ithaca. Birds of North America Online. Available from http://bna.birds.cornell.edu

  • Lowther PE (2013) Lists of victims and hots of the parasitic cowbirds (Molothrus). Available from http://www.fieldmuseum.org/sites/default/files/Molothrus_hosts-26aug2013.pdf. Accessed 27 October 2013

  • Marchetti K (2000) Egg rejection in a passerine bird: size does matter. Anim Behav 59:877–883

    Article  PubMed  Google Scholar 

  • Mermoz ME, Ornelas JF (2004) Phylogenetic analysis of life-history adaptations in parasitic cowbirds. Behav Ecol 15:109–119

    Article  Google Scholar 

  • Moksnes A, Røskaft E (1995) Egg-morphs and host preference in the common cuckoo (Cuculus canorus): an analysis of cuckoo and host eggs from European museum collections. J Zool 236:625–648

    Article  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, Sze'kely T, Kisbenedek T, Karcza Z, Ba'rtol I (2003a) The importance of nest cleaning in egg rejection behavior of great reed warblers Acrocephalus arundinaceus. J Avian Biol 34:16–19

    Google Scholar 

  • Moskát C, Karcza Z, Csörgö T (2003b) Egg rejection in European Blackbirds (Turdus merula): the effect of mimicry. Ornis Fennica 80:86–91

    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

    Google Scholar 

  • Moskát C, Bán M, Szekely T, Komdeur J, Lucassen RWG, Van Boheemen LA, 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 

  • Mullen P, Pohland G (2008) Studies on UV reflection in feathers of some 1000 bird species: are UV peaks in feathers correlated with violet-sensitive and ultraviolet-sensitive cones? Ibis 150:59–68

    Article  Google Scholar 

  • Munoz AR, Altamirano M, Takasu F, Nakamura H (2007) Nest light environment and the potential risk of Common Cuckoo (Cuculus canorus) parasitism. Auk 124:619–627

    Google Scholar 

  • Øien JI, 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, Vorobyev M (1996) Color vision as an adaptation to frugivory in primates. Proc R Soc Lond B 263:593–599

    Article  CAS  Google Scholar 

  • Parrish JW, Ptacek JA, Will KL (1984) The detection of near-ultraviolet light by nonmigratory and migratory birds. Auk 101:53–58

    Google Scholar 

  • Payne RB (1977) The ecology of brood parasitism in birds. Annu Rev Ecol Syst 8:1–28

    Article  Google Scholar 

  • Payne RB, Payne LL (1997) Brood parasitism by cowbirds : risks and effects on reproductive success and survival in indigo buntings. Behav Ecol 9:64–73

    Article  Google Scholar 

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

    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 

  • Rasmussen JL, Sealy SG, Underwood TJ (2009) Video recording reveals the method of ejection of  brown-headed cowbird eggs and no cost in American Robins and Gray Catbirds. Condor 11:570–574

    Google Scholar 

  • Røskaft E, Orians GH, Beletsky LD (1990) Why do red-winged blackbirds accept the eggs of brown-headed cowbirds? Evol Ecol 4:35–42

    Article  Google Scholar 

  • Rothstein SI (1975) An experimental and teleonomic investigation of avian brood parasitism. Condor 77:250–271

    Article  Google Scholar 

  • Rothstein SI (1982) Mechanisms of avian egg recognition: which egg parameters elicit responses by rejector 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) The evolution and ecology of avian brood parasitism. In: Rothstein SI, Robinson SK (eds) Parasitic birds and their hosts: studies in coevolution. Oxford University Press, New York, pp 3–56

    Google Scholar 

  • Sallabanks R, James FC (1999) American Robin (Turdus migratorius). In: Poole (ed) The Birds of North America Online. Cornell Lab of Ornithology, Ithaca. Birds of North America Online. Available from http://bna.birds.cornell.edu/bna/species/462

  • 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 

  • Sealy SG (1992) Removal of Yellow Warbler eggs in association with cowbird parasitism. Condor 94:40–54

    Google Scholar 

  • Sheldon BC, Andersson S, Griffith SC, et al. (1999) Ultraviolet colour variation influences blue tit sex ratios. Nature 402:874–877

    Google Scholar 

  • Slagsvold T (1998) On the origin and rarity of interspecific nest parasitism in birds. Am Nat 152:264–272

    Article  CAS  PubMed  Google Scholar 

  • Spottiswoode CN, Stevens M (2010) How to evade a coevolving brood parasite: egg discrimination versus egg variability as host defences. Proc R Soc Lond B 278:3566–3573

    Article  Google Scholar 

  • Stevens M, Troscianko J, Spottiswoode CN (2013) Repeated targeting of the same hosts be a brood parasite compromises host egg rejection. Nature Comm 4:2745

    Google Scholar 

  • Stoddard MC, Kilner RM (2013) The past, present and future of ‘cuckoos versus reed warblers’. Anim Behav 85:693–699

    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 Lond B 277:1387–1393

    Article  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 

  • Takasu F (1998) Why do all host species not show defense against avian brood parasitism: evolutionary lag or equilibrium? Am Nat 151:193–205

    Article  CAS  PubMed  Google Scholar 

  • Underwood TJ, Sealy SG (2006) Influence of shape on egg discrimination in American robins and grey catbirds. Ethology 122:164–173

    Article  Google Scholar 

  • Underwood TJ, Sealy SG (2008) UV reflectance of eggs of Brown-headed Cowbird (Molothrus ater) and accepter and rejecter hosts. J Ornithol 149:313–321

    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

    Google Scholar 

  • Voelker GS, Rohwer R, Bowie K, Outlaw DC (2007) Molecular systematics of a speciose, cosmopolitan songbird genus: defining the limits of, and relationships among, the Turdus thrushes. Mol Phylogenet Evol 42:422–434

    Article  CAS  PubMed  Google Scholar 

  • Vorobyev M, Osorio D (1998) Receptor noise as a determinant of color thresholds. Proc R Soc Lond B Bio 265:351–358

    Article  CAS  Google Scholar 

  • Vorobyev M, Osorio D, Bennett ATD, Marshall NJ, Cuthill IC (1998) Tetrachromacy, oil droplets and bird plumage colors. J Comp Physiol A 183:621–633

    Article  CAS  PubMed  Google Scholar 

  • Wagner GF, Aidala Z, Croston R, Hauber ME (2013) Repeated brood parasitism by brown-headed cowbirds (Molothrus ater) at Eastern Phoebe (Sayornis phoebe) nesting sites across non-consecutive years. Wilson J Ornithol 125:389–394

    Article  Google Scholar 

  • Welbergen J, Komdeur J, Kats R, Berg M (2001) Egg discrimination in the Australian reed warbler (Acrocephalus australis): rejection response toward model and conspecific eggs depending on timing and mode of artificial parasitism. Behav Ecol 12:8–15

    Article  Google Scholar 

Download references

Acknowledgments

For financial support, the authors thank the CUNY Graduate Center, American Ornithologists’ Union, Animal Behavior Society, the PSC-CUNY grant scheme, and the Human Frontier Science Program. For discussions and assistance, the authors also thank Zachary Aidala, Jennifer Basil, Phill Cassey, Tomas Grim, Brani Igic, David Lahti, Lisa Manne, Csaba Moskát, Lainga Tong, Michael Webster, and Sarah Woolley.

Ethical standards

This study was conducted on private land with the express permission of landowners and following the protocols and permissions of institutional and governmental agencies. The protocol was approved by the Institutional Animal Care and Use Committed of Hunter College (# MH 2/13-T3).

Author information

Authors and Affiliations

  1. Doctoral Program in Biology, Subprogram in Ecology, Evolutionary Biology and Behavior, The Graduate Center, City University of New York, New York, NY, 10016, USA

    Rebecca Croston & Mark E. Hauber

  2. Department of Psychology, Hunter College and Doctoral Program in Psychology, The Graduate Center, City University of New York, New York, NY, 10065, USA

    Mark E. Hauber

  3. c/o Hauber Lab, Department of Psychology, Hunter College, 695 Park Avenue, New York, NY, 10065, USA

    Rebecca Croston

Authors
  1. Rebecca Croston
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mark E. Hauber
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Rebecca Croston.

Additional information

Communicated by M. Soler

Rights and permissions

Reprints and permissions

About this article

Cite this article

Croston, R., Hauber, M.E. Spectral tuning and perceptual differences do not explain the rejection of brood parasitic eggs by American robins (Turdus migratorius). Behav Ecol Sociobiol 68, 351–362 (2014). https://doi.org/10.1007/s00265-013-1649-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-013-1649-8

Keywords

Search

Navigation