The Science of Nature

, 104:14 | Cite as

A test of the nest sanitation hypothesis for the evolution of foreign egg rejection in an avian brood parasite rejecter host species

  • Alec B. Luro
  • Mark E. Hauber
Original Paper


Hosts of avian brood parasites have evolved diverse defenses to avoid the costs associated with raising brood parasite nestlings. In egg ejection, the host recognizes and removes foreign eggs laid in its nest. Nest sanitation, a behavior similar in motor pattern to egg ejection, has been proposed repeatedly as a potential pre-adaptation to egg ejection. Here, we separately placed blue 3D-printed, brown-headed cowbird (Molothrus ater) eggs known to elicit interindividual variation in ejection responses and semi-natural leaves into American robins’ (Turdus migratorius) nests to test proximate predictions that (1) rejecter hosts should sanitize debris from nests more frequently and consistently than accepter hosts and (2) hosts that sanitize their nests of debris prior to the presentation of a foreign egg will be more likely to eject the foreign egg. Egg ejection responses were highly repeatable within individuals yet variable between them, but were not influenced by prior exposure to debris, nor related to sanitation tendencies as a whole, because nearly all individuals sanitized their nests. Additionally, we collected published data for eight different host species to test for a potential positive correlation between sanitation and egg ejection. We found no significant correlation between nest sanitation and egg ejection rates; however, our comparative analysis was limited to a sample size of 8, and we advise that more data from additional species are necessary to properly address interspecific tests of the pre-adaptation hypothesis. In lack of support for the nest sanitation hypothesis, our study suggests that, within individuals, foreign egg ejection is distinct from nest sanitation tendencies, and sanitation and foreign egg ejection may not correlate across species.


Nest sanitation Egg rejection Brood parasitism Turdus migratorius 



We thank Moore’s Tree Farm; Seifert’s Tree Farm; and Country Arbors Nursery of Champaign-Urbana, IL, for generously providing access to their farms as field sites for this study and Matt Louder for facilitating the preliminary field work. We also thank Thomas A. Gavin, Professor Emeritus, Cornell University, for the help with editing the English in this paper. Lastly, we thank Professor David Lahti of Queen’s College for the thoughtful comments and suggestions which improved the manuscript. Funding for this project was provided by the Human Frontier Science Program, the National Academies Keck Future Initiative program, and the Animal Behavior and Conservation program of Hunter College. A. Luro was supported in part by the Department of Animal Biology, University of Illinois at Urbana-Champaign, fellowship during the preparation of this manuscript.

Compliance with ethical standards

Ethical standards

All experiments and procedures of this study were IUACUC approved (MH 2/16-T3) and complied with US laws.

Conflict of interest

The authors declare they have no conflict of interest.

Supplementary material

114_2017_1446_MOESM1_ESM.xlsx (18 kb)
ESM 1 (XLSX 18 kb)


  1. Aidala Z, Croston R, Schwartz J, Tong L, Hauber ME (2015) The role of egg–nest contrast in the rejection of brood parasitic eggs. J Exp Biol 218:1126–1136CrossRefPubMedGoogle Scholar
  2. Amundsen T, Brobakken PT, Moksnes A, Røskaft E (2002) Rejection of cuckoo Cuculus canorus eggs in relation to female age in the bluethroat (Luscinia svecica). J Avian Biol 33:366–370CrossRefGoogle Scholar
  3. Ankney CD, Johnson SL (1985) Variation in weight and composition of brown-headed cowbird eggs. Condor 87:296–299CrossRefGoogle Scholar
  4. Bán 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 24:1014–1021CrossRefGoogle Scholar
  5. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Statistical Software 67(1):1–48. doi: 10.18637/jss.v067.i01 CrossRefGoogle Scholar
  6. Blair RH, Tucker BW (1941) Nest sanitation. Brit Birds 34:206–255Google Scholar
  7. Briskie JV, Sealy SG, Hobson KA (1992) Behavioral defenses against avian brood parasitism in sympatric and allopatric host populations. Evolution 46:334–340CrossRefGoogle Scholar
  8. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information theoretic approach. Springer Verlag, New YorkGoogle Scholar
  9. Core Team R (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna URL Google Scholar
  10. Croston R, Hauber ME (2014a) Spectral tuning and perceptual differences do not explain the rejection of brood parasitic eggs by American robins (Turdus migratorius). Behav Ecol Sociobiol 68:351–362CrossRefGoogle Scholar
  11. Croston R, Hauber ME (2014b) High repeatability of egg rejection in response to experimental brood parasitism in the American robin (Turdus migratorius). Behaviour 151:703–718CrossRefGoogle Scholar
  12. Davies NB (2000) Cuckoos, cowbirds and other cheats. Poyser, LondonGoogle Scholar
  13. Davies NB, Brooke MDL, Kacelnik A (1996) Recognition errors and probability of parasitism determine whether reed warblers should accept or reject mimetic cuckoo eggs. P R Soc B 263:925–931CrossRefGoogle Scholar
  14. Dukas R (2004) Evolutionary biology of animal cognition. Ann Rev Ecol Evol S34:347–374CrossRefGoogle Scholar
  15. Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15CrossRefGoogle Scholar
  16. Gamer M, Lemon J, Fellows I, Singh P (2012) irr: various coefficients of interrater reliability and agreement. R package version 0.84.
  17. Garland T, Harvey PH, Ives AR (1992) Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst Biol 41:18–32CrossRefGoogle Scholar
  18. Gould SJ, Vrba ES (1982) Exaptation—a missing term in the science of form. Paleobiology 8:4–15CrossRefGoogle Scholar
  19. Guigueno MF, Sealy SG (2009) Nest sanitation plays a role in egg burial by yellow warblers. Ethology 115:247–256CrossRefGoogle Scholar
  20. Guigueno MF, Sealy SG (2012) Nest sanitation in passerine birds: implications for egg rejection in hosts of brood parasites. J Ornithol 153:35–52CrossRefGoogle Scholar
  21. Hanley D, Samaš P, Heryán J, Hauber ME, Grim T (2015) Now you see it, now you don’t: flushing hosts prior to experimentation can predict their responses to brood parasitism. Scientific Reports 5:9060CrossRefPubMedPubMedCentralGoogle Scholar
  22. Hauber ME (2003) Egg-capping is a cost paid by hosts of interspecific brood parasites. Auk 120:860–865CrossRefGoogle Scholar
  23. Hauber ME, Tong L, Bán M, Croston R, Grim T, Waterhouse GIN, Shawkey MD, Barron AB, Moskát C (2015) The value of artificial stimuli in behavioral research: making the case for egg rejection studies in avian brood parasitism. Ethology 121:521–528CrossRefGoogle Scholar
  24. Honza M, Kuiper SM, Cherry MI (2005) Behaviour of African turdid hosts towards experimental parasitism with artificial red-chested cuckoo (Cuculus solitaries) eggs. J Avian Biol 36:517–522CrossRefGoogle Scholar
  25. Honza M, Polačiková L, Procházka P (2007) Ultraviolet and green parts of the colour spectrum affect egg rejection in the song thrush (Turdus philomelos). Biol J Linn Soc 92:269–276CrossRefGoogle Scholar
  26. Howell JC (1942) Notes on the nesting habits of the American Robin (Turdus migratorius). Am Midl Nat 28:529–603CrossRefGoogle Scholar
  27. Igic B, Nunez V, Voss HU, Croston R, Aidala Z, López AV, Tatenhove AV, Hoford ME, Shawkey MD, Hauber ME (2015) Using 3D printed eggs to examine the egg-rejection behaviour of wild birds. Peer J 3:e965CrossRefPubMedPubMedCentralGoogle Scholar
  28. Jetz W, Thomas GH, Joy JB, Hartmann K, Mooers AO (2012) The global diversity of birds in space and time. Nature 491:444–448CrossRefPubMedGoogle Scholar
  29. Lahti DC (2015) The limits of artificial stimuli in behavioral research: the umwelt gamble. Ethology 121:529–537CrossRefGoogle Scholar
  30. Liang W, Yang C, Wang L, Møller AP (2013) Avoiding parasitism by breeding indoors: cuckoo parasitism of hirundines and rejection of eggs. Behav Ecol Sociobiol 67(6):913–918Google Scholar
  31. Maddison WP, Maddison DR (2016) Mesquite: a modular system for evolutionary analysis. Version 3.11
  32. Martin K (1973) Breeding density and reproductive success of robins in relation to habitat structure on logged areas of Vancouver Island, British Columbia. Master’s Thesis, University of Alberta, Edmonton, ABGoogle Scholar
  33. Medina I, Langmore NE (2016) The evolution of acceptance and tolerance in hosts of avian brood parasites. Biol Rev 91:569–577CrossRefPubMedGoogle Scholar
  34. Mendelson TC, Fitzpatrick CL, Hauber ME, Pence CH, Rodríguez RL, Safran RJ, Stern CA, Stevens JR (2016) Cognitive phenotypes and the evolution of animal decisions. Trends Ecol Evol 31:850–859CrossRefPubMedGoogle Scholar
  35. Moskát C, Székely T, Kisbenedek T, Karcza Z, Bártol I (2003a) The importance of nest cleaning in egg rejection behaviour of great reed warblers (Acrocephalus arundinaceus). J Avian Biol 34:16–19CrossRefGoogle Scholar
  36. Moskát C, Karcza Z, Csorgo T (2003b) Egg rejection in European blackbirds (Turdus merula): the effect of mimicry. Ornis Fennica 80:86–91Google Scholar
  37. Ortega CP, Cruz A (1988) Mechanisms of egg acceptance by marsh-dwelling blackbirds. Condor 90:349–358CrossRefGoogle Scholar
  38. Palomino J, Martin-Vivaldi M, Soler M, Soler JJ (1998) Females are responsible for ejection of cuckoo eggs in the rufous bush robin. Anim Behav 56:131–136CrossRefPubMedGoogle Scholar
  39. Payne RB (1977) The ecology of brood parasitism in birds. Ann Rev Ecol Syst 8:1–28CrossRefGoogle Scholar
  40. Peer BD, Rothstein SI (2010) Phenotypic plasticity in common grackles (Quiscalus quiscula) in response to repeated brood parasitism. Auk 127:293–299CrossRefGoogle Scholar
  41. Peer BD, Sealy SG (2004) Correlates of egg rejection in hosts of the brown-headed cowbird. Condor 106:580–599CrossRefGoogle Scholar
  42. Poláček M, Griggio M, Bartíková M, Hoi H (2013) Nest sanitation as the evolutionary background for egg ejection behaviour and the role of motivation for object removal. PLoS One 8:e78771CrossRefPubMedPubMedCentralGoogle Scholar
  43. 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 111:570–574CrossRefGoogle Scholar
  44. Røskaft E, Moksnes A, Meilvang D, Bicík V, Jemelíková J, Honza M (2002) No evidence for recognition errors in Acrocephalus warblers. J Avian Biol 33:31–38CrossRefGoogle Scholar
  45. Rothstein SI (1970) An experimental investigation of the defenses of the hosts of the parasitic brown-headed cowbird (Molothrus ater). Doctoral dissertation, Yale UniversityGoogle Scholar
  46. Rothstein SI (1975a) An experimental and teleonomic investigation of avian brood parasitism. Condor 77:250–271CrossRefGoogle Scholar
  47. Rothstein SI (1975b) Evolutionary rates and host defenses against avian brood parasitism. Am Nat 109:161–176CrossRefGoogle Scholar
  48. Rothstein SI (1982) Mechanisms of avian egg recognition: which egg parameters elicit responses by rejecter species? Behav Ecol Sociobiol 11:229–239CrossRefGoogle Scholar
  49. Samaš P, Hauber ME, Cassey P, Grim T (2011) Repeatability of foreign egg rejection: testing the assumptions of co-evolutionary theory. Ethology 117:606–619CrossRefGoogle Scholar
  50. Sauer JR, Hines JE, Fallon JE, Pardieck KL, Ziolkowski DJ, Link WA (2014) The North American breeding bird survey, results and analysis 1966–2013. Version 01.30.2015. USGS Patuxent Wildlife Research Center, LaurelGoogle Scholar
  51. Soler M, Martin-Vivaldi M, Perez-Contreras T (2002) Identification of the sex responsible for recognition and the method of ejection of parasitic eggs in some potential common cuckoo hosts. Ethology 108:1093–1101CrossRefGoogle Scholar
  52. Thomson DF (1934) Some adaptations for the disposal of fæces. The hygiene of the nest in Australian birds. P Zool Soc Lond 104:701–708CrossRefGoogle Scholar
  53. Tinbergen N, Broekhuysen GJ, Feekes F, Houghton JCW, Kruuk H, Szulc E (1962) Egg shell removal by the black-headed gull, Larus ridibundus L: a behaviour component of camouflage. Behaviour 19:74–116CrossRefGoogle Scholar
  54. Underwood TJ, Sealy SG (2006) Influence of shape on egg discrimination in American robins and gray catbirds. Ethology 112:164–173CrossRefGoogle Scholar
  55. Wallace GJ, Mahan HD (1975) An introduction to ornithology, 3rd edn. Macmillan, New YorkGoogle Scholar
  56. Wolak ME, Fairbairn DJ, Paulsen YR (2012) Guidelines for estimating repeatability. Methods Ecol Evol 3:129–137CrossRefGoogle Scholar
  57. Yang C, Wang L, Møller AP (2015a) Nest sanitation behavior in hirundines as a pre-adaptation to egg rejection to counter brood parasitism. Anim Cogn 18:355–360CrossRefPubMedGoogle Scholar
  58. Yang C, Wang L, Møller AP (2015b) Nest sanitation elicits egg discrimination in cuckoo hosts. Anim Cogn 18:1373–1377CrossRefPubMedGoogle Scholar
  59. Young H (1955) Breeding behavior and nesting of the eastern robin. Am Midl Nat 53:329–352CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Animal Behavior and Conservation Program, Department of PsychologyHunter College of the City University of New YorkNew YorkUSA
  2. 2.Department of Animal Biology, School of Integrative BiologyUniversity of Illinois at Urbana-ChampaignChampaignUSA

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