Journal of Ornithology

, Volume 153, Issue 2, pp 467–475 | Cite as

Indirect estimates of breeding and natal philopatry in an obligate avian brood parasite

  • Mark E. Hauber
  • Bill M. Strausberger
  • Kevin A. Feldheim
  • Justin Lock
  • Phillip Cassey
Original Article


In theory, obligate brood parasitic birds are freed from several of the temporal and spatial constraints of parental care for dependent young. Yet, similar to parental bird species, adults in several avian brood parasites show a territorial spacing system while breeding, including site fidelity within and across years. Banding-based capture and sighting studies are also suggestive of non-parasite-like lower levels of natal philopatry in avian brood parasites. We analyzed the potential correlation of physical distance with genetic structure of a Brown-headed Cowbird Molothrus ater population, sampling parasitic chicks from nests across different temporal and spatial scales of its common host, the Eastern Phoebe Sayornis phoebe, near Ithaca, New York, USA. In support of extensive breeding but not historical patterns of natal philopatry, we detected no significant covariation of genetic similarity by distance of nestling parasites at the scale beyond that of individual host nest sites. These results contribute towards a baseline for future behavioral and genetic comparisons of whether and how parasitic versus parental reproductive strategies impact patterns of avian population genetic structure across space and time.


Breeding range Brood parasite Dispersal Site fidelity Territoriality 


Indirekte Bewertung von Brüten und angeborener Ortstreue bei einem obligatorischen Brutparasiten

Theoretisch unterliegen obligate Brutparasiten nicht all‘ den zeitlichen und räumlichen Zwängen von Vögeln, die für ihre Jungen Brutpflege leisten. Dennoch zeigen adulte Tiere einiger Brutparasiten-Arten während der Brutzeit ein territoriales Verhalten, zu dem, ähnlich den brutpflegenden Vogelarten, Ortstreue innerhalb eines Jahres und über mehrere Jahre hinweg gehört. Auch Beobachtungen und Fänge beringter Tiere weisen auf niedrigere Stufen angeborener Ortstreue bei Brutparasiten hin. In unserer Studie analysierten wir für Populationen des Braunkopf-Kuhstärlings (Molothrus ater) mögliche Korrelationen von räumlichen Abständen mit genetischer Ähnlichkeit, indem wir in der Nähe von Ithaca, New York, in unterschiedlichen räumlichen und zeitlichen Maßstäben Parasiten-Küken aus Nestern ihres üblichen Wirtsvogels, des Weißbauch-Phoebetyranns (Sayornis phoebe), untersuchten. Wir fanden keine signifikante Kovarianz von genetischer Ähnlichkeit mit räumlicher Verteilung. Dieses Ergebnis bildet einen Ausgangspunkt für zukünftige vergleichende verhaltensbiologische und genetische Untersuchungen der Frage, ob und inwieweit parasitische versus brutpflegerische Fortpflanzungsstrategien einen Einfluss auf die genetische Struktur von Vogelpopulationen in Zeit und Raum haben.



Funding was provided by the Howard Hughes Medical Institute (to M.E.H.), the Human Frontier Science Program (to M.E.H. and P.C.), the Miller Institute of UC Berkeley (to M.E.H.) and the PSC-CUNY grant award scheme (to M.E.H.). Molecular work was conducted in the Pritzker Laboratory for Molecular Systematics and Evolution, operated with support from the Pritzker Foundation. For discussions and comments we are grateful to C. Tonra, R. Fleischer, S. Heath, E. A. Lacey, C. Millar, J. Oursler, and many other colleagues. This research was approved by federal, state, and institutional animal ethics protocols.


  1. Alderson GW, Gibbs HL, Sealy SG (1999) Parentage and kinship analyses in an obligate brood parasitic bird, the brown-headed cowbird (Molothrus ater) using microsatellite DNA markers. J Hered 90:182–190PubMedCrossRefGoogle Scholar
  2. Anderson KE, Rothstein SI, Fleischer RC, O’Loghlen AL (2005) Large-scale movement patterns between song dialects in brown-headed cowbirds (Molothrus ater). Auk 122:803–818CrossRefGoogle Scholar
  3. Arcese P, Smith JNM, Hatch JI (1996) Nest predation by cowbirds, and its consequences for passerine demography. Proc Natl Acad Sci USA 93:4608–4611PubMedCrossRefGoogle Scholar
  4. Daniel C, Millar CD, Ismar SMH, Stephenson B, Hauber ME (2007) Evaluating molecular and behavioural sexing methods for the Australasian gannet (Morus serrator). Aust J Zool 55:377–382 CrossRefGoogle Scholar
  5. Darley JA (1982) Territoriality and mating behavior of the male brown-headed cowbird. Condor 84:15–21CrossRefGoogle Scholar
  6. Darley JA (1983) Territorial behavior of the brown-headed cowbird. Can J Zool 61:65–69CrossRefGoogle Scholar
  7. Davies NB (2000) Cuckoos, cowbirds and other cheats. Poyser, LondonGoogle Scholar
  8. Double MC, Peakall R, Beck NR, Cockburn A (2005) Dispersal, philopatry, and infidelity: dissecting local genetic structure in superb fairy-wrens (Malurus cyaneus). Evolution 59:625–635PubMedGoogle Scholar
  9. Dufty AM (1982) Movements and activities of radio-tracked brown-headed cowbirds. Auk 99:316–327Google Scholar
  10. Dufty AM (1988) The effects of repeated blood sampling on survival in brown-headed cowbirds. Condor 90:939–941CrossRefGoogle Scholar
  11. Dutech C, Sork VL, Irwin AJ, Smouse PE, Davis FW (2005) Gene flow and fine-scale genetic structure in a wind-pollinated tree species, Quercus lobata (Fagaceaee). Am J Bot 92:252–261PubMedCrossRefGoogle Scholar
  12. Ellison K, Sealy SG, Gibbs HL (2006) Genetic elucidation of host use by individual sympatric bronzed cowbirds (Molothrus aeneus) and brown-headed cowbirds (M. ater). Can J Zool 84:1269–1280CrossRefGoogle Scholar
  13. Fleischer RC (1985) A new technique to identify and assess the dispersion of eggs of individual brood parasites. Behav Ecol Sociobiol 17:91–99Google Scholar
  14. Fleischer RC, Rothstein SI (1988) Known secondary contact and rapid gene flow among subspecies and dialects in the brown-headed cowbird. Evolution 42:1146–1158CrossRefGoogle Scholar
  15. Fleischer RC, Rothstein SI, Miller LS (1991) Mitochondrial DNA variation indicates gene flow across a zone of known secondary contact between two subspecies of the brown-headed cowbird. Condor 93:185–189CrossRefGoogle Scholar
  16. Fossoy F, Antonov A, Moksnes A, Roskaft E, Vikan JR, Moller AP, Shykoff JA, Stokke BG (2011) Genetic differentiation among sympatric cuckoo host races: males matter. Proc R Soc Lond B 278:1639–1645CrossRefGoogle Scholar
  17. Friedmann H (1929) The cowbirds: a study in the biology of the social parasitism. Thomas, SpringfieldGoogle Scholar
  18. Gibbs HL, Miller P, Alderson GW, Sealy SG (1997) Genetic analysis of brown-headed cowbirds Molothrus ater raised by different hosts: data from mtDNA and microsatellite DNA markers. Mol Ecol 6:189–193CrossRefGoogle Scholar
  19. Gibbs HL, Sorenson MD, Marchetti K, Brooke MDL, Davies NB, Nakamura H (2000) Genetic evidence for female host-specific races of the common cuckoo. Nature 407:183–186PubMedCrossRefGoogle Scholar
  20. Goodnight KF, Queller DC (1999) Computer software for performing likelihood tests of pedigree relationships using genetic markers. Mol Ecol 8:1231–1234CrossRefGoogle Scholar
  21. Grim T (2002) Why is mimicry in cuckoo eggs sometimes so poor? J Avian Biol 33:302–305CrossRefGoogle Scholar
  22. Hahn DC, Fleischer RC (1995) DNA fingerprint similarity between female and juvenile brown-headed cowbirds trapped together. Anim Behav 49:1577–1580 CrossRefGoogle Scholar
  23. Hahn DC, Sedgwick J, Painter I, Carna NJ (1999) A spatial and genetic analysis of cowbird host selection. Stud Avian Biol 18:204–217Google Scholar
  24. Hauber ME (2000) Nest predation and cowbird parasitism in song sparrows. J Field Ornithol 71:389–398Google Scholar
  25. Hauber ME (2001) Site selection and repeatability in brown-headed cowbird (Molothrus ater) parasitism of eastern phoebe (Sayornis phoebe) nests. Can J Zool 79:1518–1523Google Scholar
  26. Hauber ME (2002) First contact: a role for adult-offspring social association in the species recognition system of brood parasites. Ann Zool Fenn 39:291–305Google Scholar
  27. Hauber ME (2003) Hatching asynchrony, nestling competition, and the cost of interspecific brood parasitism. Behav Ecol 14:224–235CrossRefGoogle Scholar
  28. Hauber ME, Dearborn DC (2003) Parentage without parental care: what to look for in genetic studies of obligate brood-parasitic mating systems. Auk 120:1–13CrossRefGoogle Scholar
  29. Hauber ME, Russo SA (2000) Perch proximity correlates with higher rates of cowbird parasitism of ground nesting song sparrows. Wilson Bull 112:150–153CrossRefGoogle Scholar
  30. Hauber ME, Russo SA, Sherman PW (2001) A password for species recognition in a brood parasitic bird. Proc R Soc Lond B 268:1041–1048CrossRefGoogle Scholar
  31. Hauber ME, Sherman PW, Paprika D (2000) Self-referent phenotype matching in a brood parasite: the armpit effect in brown-headed cowbirds (Molothrus ater). Anim Cognit 3:113–117 Google Scholar
  32. Hauber ME, Yeh PJ, Roberts JOL (2004) Patterns and coevolutionary consequences of repeated brood parasitism. Proc R Soc Lond B 271:S317–S320CrossRefGoogle Scholar
  33. Hoover JP (2003) Multiple effects of brood parasitism reduce the reproductive success of prothonotary warblers, Protonotaria citrea. Anim Behav 65:923–934CrossRefGoogle Scholar
  34. Hoover JP, Hauber ME (2007) Individual patterns of habitat and nest-site use by hosts promote transgenerational transmission of avian brood parasitism status. J Anim Ecol 76:1208–1214PubMedCrossRefGoogle Scholar
  35. Hoover JP, Reetz MJ (2006) Brood parasitism increases provisioning rate, and reduces offspring recruitment and adult return rates, in a cowbird host. Oecologia 149:165–173PubMedCrossRefGoogle Scholar
  36. Hoover JP, Yasukawa K, Hauber ME (2006) Spatial and temporal structure of avian brood parasitism affects the fitness benefits of egg ejection and nest abandonment. Anim Behav 72:881–890CrossRefGoogle Scholar
  37. Kilner RM, Madden JR, Hauber ME (2004) Brood parasitic cowbirds use host young to procure food. Science 305:877–879PubMedCrossRefGoogle Scholar
  38. Langmore NE, Adcock GJ, Kilner RM (2007) The spatial organization and mating system of the Horsfield’s bronze-cuckoo Chalcites basalis. Anim Behav 74:403–412CrossRefGoogle Scholar
  39. Lapointe FJ, Legendre P (1992) A statistical framework to test the consensus among additive trees (cladograms). Syst Biol 41:158–171Google Scholar
  40. Lawes MJ, Marthews TR (2003) When will rejection of parasite nestlings by hosts of non-evicting avian brood parasites be favored? A misimprinting-equilibrium model. Behav Ecol 14:757–770 Google Scholar
  41. Longmire JL, Roach JL, Maltbie M, White PS, Tatum OL, Makova KD, Hahn DC (2001) Tetranucleotide microsatellite markers for the brown-headed cowbird (Molothrus ater). J Avian Biol 32:76–78CrossRefGoogle Scholar
  42. Lotem A (1993) Learning to recognize nestlings is maladaptive for cuckoo Cuculus canorus hosts. Nature 362:743–745Google Scholar
  43. Lyon BE (1997) Spatial patterns of Shiny cowbird brood parasitism on chestnut-capped blackbirds. Anim Behav 54:927–939PubMedCrossRefGoogle Scholar
  44. Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Res 27:209–220PubMedGoogle Scholar
  45. Marchetti K, Nakamura KH, Gibbs HL (1998) Host race formation in the common cuckoo. Science 282:471–472PubMedCrossRefGoogle Scholar
  46. May RM, Robinson SK (1985) Population dynamics of avian brood parasitism. Am Nat 126:475–494CrossRefGoogle Scholar
  47. McLaren CM, Woolfenden BE, Gibbs HL, Sealy SG (2003) Genetic and temporal patterns of multiple parasitism by brown-headed cowbirds (Molothrus ater) on song sparrows (Melospiza melodia). Can J Zool 81:281–286CrossRefGoogle Scholar
  48. Nice MM (1937) Studies in the life history of the song sparrow, vol I. Dover, New YorkGoogle Scholar
  49. Nice MM (1939) Observations on the behavior of a young cowbird. Wilson Bull 51:233–239Google Scholar
  50. O’Loghlen AL, Rothstein SI (2002) Vocal development is correlated with an indicator of hatching date inbrown-headed cowbirds. Condor 104:761–771CrossRefGoogle Scholar
  51. Ortega CP (1998) Cowbirds and other brood parasites. The University of Arizona Press, Tucson Google Scholar
  52. Ortega JP, Ortega CP (2009) Sex ratios and survival probablities of brown-headed cowbirds (Molothrus ater) in Southwest Colorado. Auk 126:268–277CrossRefGoogle Scholar
  53. Ortego J, Calabuig G, Aparicio JM, Cordero PJ (2008) Genetic consequences of natal dispersal in the colonial lesser kestrel. Mol Ecol 17:2051–2059PubMedCrossRefGoogle Scholar
  54. Pearce JM (2007) Philopatry: a return to origins. Auk 124:1085–1087CrossRefGoogle Scholar
  55. Queller DD, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275CrossRefGoogle Scholar
  56. Raim A (2000) Spatial patterns of breeding female brown-headed cowbirds on an Illinois site. In: Smith JNM, Cook TL, Rothstein SI, Robinson SK, Sealy SG (eds) Ecology and management of cowbirds and their hosts: studies in the conservation of North American Passerine Birds. University of Texas Press, Austin, pp 87–99Google Scholar
  57. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  58. Richardson K, Ewen JG, Armstrong DP, Hauber ME (2010) Sex-specific shifts in natal dispersal dynamics in a reintroduced hihi population. Behaviour 147:1517–1532CrossRefGoogle Scholar
  59. Robinson SK, Thompson FR III, Donovan TM, Whithead M, Faaborg J (1995) Regional forest fragmentation and the nesting success of migratory birds. Science 267:1987–1990PubMedCrossRefGoogle Scholar
  60. Roskaft E, Moksnes A, Stokke BG, Moskat C, Honza M (2002) The spatial habitat structure of host populations explains the pattern of rejection behavior in hosts and parasitic adaptations in cuckoos. Behav Ecol 13:163–168CrossRefGoogle Scholar
  61. Rothstein SI, Yokel DA, Fleischer RC (1986) Mating and spacing systems, female fecundity and vocal dialects in captive and free-ranging brown-headed cowbirds. Curr Ornithol 3:127–185Google Scholar
  62. Schlossberg S (2009) Site fidelity of shrubland and forest birds. Condor 111:238–246CrossRefGoogle Scholar
  63. Smith JNM, Arcese P (1994) Brown-headed cowbirds and an island population of song sparrows: a 16-year study. Condor 96:916–934CrossRefGoogle Scholar
  64. Soler M, Soler JJ (1999) Innate versus learned recognition of conspecifics in great spotted cuckoos (Clamator glandarius). Anim Cognit 2:97–102 CrossRefGoogle Scholar
  65. Soler M, Soler JJ, Martinez JG, Moller AP (1995) Magpie host manipulation by great spotted cuckoos: evidence for an avian mafia? Evolution 49:770–775CrossRefGoogle Scholar
  66. Strausberger BM, Ashley MV (1997) Community-wide patterns of parasitism of a host “generalist” brood-parasitic cowbird. Oecologia 112:254–262CrossRefGoogle Scholar
  67. Strausberger BM, Ashley MV (2001) Eggs yield nuclear DNA from egg-laying female cowbirds, their embryos, and offspring. Conserv Gen 2:385–390CrossRefGoogle Scholar
  68. Strausberger BM, Ashley MV (2003) Breeding biology of brood parasitic Brown-headed Cowbirds (Molothrus ater) characterized by parent-offspring and sibling group reconstruction. Auk 120:433–445CrossRefGoogle Scholar
  69. Strausberger BM, Ashley MV (2005) Host use strategies of individual female brown-headed cowbirds Molothrus ater in a diverse avian community. J Avian Biol 36:313–321CrossRefGoogle Scholar
  70. Strausberger BM, Rothstein SI (2009) Parasitic cowbirds may defeat host defense by causing rejecters to misimprint on cowbird eggs. Behav Ecol 20:691–699CrossRefGoogle Scholar
  71. Stutchbury BJM, Tarof SA, Done T, Gow E, Kramer PM, Tautin J, Fox JW, Afanasyev V (2009) Tracking long-distance songbird migration using geolocators. Science 323:896PubMedCrossRefGoogle Scholar
  72. Temple HJ, Hoffman JI, Amos W (2006) Dispersal, philopatry and intergroup relatedness: fine-scale genetic structure in the white-breasted thrasher, Ramphocinclus brachyurus. Mol Ecol 15:3449–3458PubMedCrossRefGoogle Scholar
  73. Tonra CM, Hauber ME, Heath SK, Johnson MD (2008) Ecological correlates and sex differences in early development of a generalist brood parasite. Auk 125:205–213CrossRefGoogle Scholar
  74. Trine CL (2000) Effects of multiple parasitism on cowbird and wood thrush nesting success. In: Smith JNM, Cook TL, Rothstein SI, Robinson SK, Sealy SG (eds) Ecology and management of cowbirds and their hosts. University of Texas Press, Austin, pp 135–144Google Scholar
  75. Weatherhead PJ, Forbes MRL (1995) Natal philopatry in passerine birds: genetic or ecological influences? Behav Ecol 5:426–433CrossRefGoogle Scholar
  76. Wikelski M, Kays RW, Kasdin J, Thorup K, Smith JA, Cochran WW, Swenson GW Jr (2007) Going wild: what a global small-animal tracking system could do for experimental biologists. J Exp Biol 210:181–186PubMedCrossRefGoogle Scholar
  77. Winkler DW, Wrege PH, Allen PE, Kast TL, Senesac P, Wasson MF, Sullivan PJ (2005) The natal dispersal of tree swallows in a continuous mainland environment. J Anim Ecol 74:1080–1090CrossRefGoogle Scholar
  78. Woolfenden BE, Gibbs HL, Sealy SG (2001) Demography of brown-headed cowbirds at Delta Marsh, Manitoba. Auk 118:156–166CrossRefGoogle Scholar
  79. Woolfenden BE, Gibbs HL, Sealy SG, McMaster DG (2003) Host use and fecundity of individual female brown-headed cowbirds. Anim Behav 65:1–11CrossRefGoogle Scholar
  80. Woxvold IA, Adcock GJ, Mulder RA (2006) Fine-scale genetic structure and dispersal in cooperatively breeding apostlebirds. Mol Ecol 15:3139–3146PubMedCrossRefGoogle Scholar

Copyright information

© Dt. Ornithologen-Gesellschaft e.V. 2011

Authors and Affiliations

  • Mark E. Hauber
    • 1
  • Bill M. Strausberger
    • 2
  • Kevin A. Feldheim
    • 2
  • Justin Lock
    • 3
  • Phillip Cassey
    • 4
  1. 1.Department of Psychology, Hunter CollegeCity University of New YorkNew YorkUSA
  2. 2.Pritzker Laboratory for Molecular Systematics and EvolutionThe Field MuseumChicagoUSA
  3. 3.Smithsonian InstitutionNational Zoological ParkWashingtonUSA
  4. 4.School of Earth and Environmental SciencesUniversity of AdelaideAdelaideAustralia

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