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Despite the costs to avian parents of rearing brood parasitic offspring, many species do not reject foreign eggs from their nests.We show that where multiple parasitism occurs, rejection itself can be costly, by increasing the risk of host egg loss during subsequent parasite attacks. Chalk-browed mockingbirds (Mimus saturninus) are heavily parasitized by shiny cowbirds (Molothrus bonariensis), which also puncture eggs in host nests. Mockingbirds struggle to prevent cowbirds puncturing and laying, but seldom remove cowbird eggs once laid. We filmed cowbird visits to nests with manipulated clutch compositions and found that mockingbird eggs were more likely to escape puncture the more cowbird eggs accompanied them in the clutch. A Monte Carlo simulation of this 'dilution effect', comparing virtual hosts that systematically either reject or accept parasite eggs, shows that acceptors enjoy higher egg survivorship than rejecters in host populations where multiple parasitism occurs. For mockingbirds or other hosts in which host nestlings fare well in parasitized broods, this benefit might be sufficient to offset the fitness cost of rearing parasite chicks, making egg acceptance evolutionarily stable. Thus, counterintuitively, high intensities of parasitism might decrease or even reverse selection pressure for host defence via egg rejection. © 2012 The Royal Society.


Documento: Artículo
Título:Brood parasite eggs enhance egg survivorship in a multiply parasitized host
Autor:Gloag, R.; Fiorini, V.D.; Reboreda, J.C.; Kacelnik, A.
Filiación:Department of Zoology, University of Oxford, South Parks Road, Oxford OX1 3PS, United Kingdom
Departamento de Ecología, Genética y Evolución, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Pabellón II Ciudad Universitaria, C1428EGA Buenos Aires, Argentina
Palabras clave:Egg rejection; Evolutionary equilibrium; Host defence; Mimus saturninus; Molothrus bonariensis; Risk dilution; brood parasitism; clutch size; defense behavior; egg rejection; Monte Carlo analysis; numerical model; parent-offspring interaction; passerine; rearing; reproductive cost; survivorship; Aves; Mimus saturninus; Molothrus; Molothrus bonariensis
Página de inicio:1831
Página de fin:1839
Título revista:Proceedings of the Royal Society B: Biological Sciences
Título revista abreviado:Proc. R. Soc. B Biol. Sci.


  • Rothstein, S.I., A model system for coevolution: Avian brood parasitism (1990) Annu. Rev. Ecol. Syst, 21, pp. 481-508. , (doi:10.1146/
  • Winfree, R., Cuckoos, cowbirds and the persistence of brood parasitism (1999) Trends Ecol. Evol, 14, pp. 338-343. , (doi:10.1016/S0169-5347(99)01643-2)
  • Langmore, N.E., Hunt, S., Kilner, R.M., Escalation of a coevolutionary arms race through host rejection of brood parasitic young (2003) Nature, 422, pp. 157-160. , (doi:10. 1038/nature01460)
  • Sato, T., Tokue, K., Noske, R.A., Mikami, O.K., Ueda, K., Evicting cuckoo nestlings from the nest: A new anti-parasitism behaviour (2010) Biol. Lett, 6, pp. 67-69. , (doi:10.1098/rsbl.2009.0540)
  • Dawkins, R., Krebs, J.R., Arms races between and within species (1979) Proc. R. Soc. Lond. B, 205, pp. 489-511. , (doi:10.1098/rspb.1979.0081)
  • Davies, N.B., Cuckoos and cowbirds versus hosts: Co-evolutionary lag and equilibrium (1999) Ostrich, 70, pp. 71-79. , (doi:10.1080/00306525.1999.9639751)
  • Langmore, N.E., Stevens, M., Maurer, G., Kilner, R.M., Are dark cuckoo eggs cryptic in host nests? (2009) Anim. Behav, 78, pp. 461-468. , (doi:10.1016/j.anbehav.2009.06.003)
  • Stoddard, M.C., Stevens, M., Avian vision and the evolution of egg color mimicry in the common cuckoo (2011) Evolution, 65, pp. 1-9. , (doi:10.1111/j.1558-5646. 2011.01262.x)
  • Spottiswoode, C.N., Stevens, M., How to evade a coevolving brood parasite: Egg discrimination versus egg variability as host defences (2011) Proc. R. Soc. B, 278, pp. 3566-3573. , (doi:10.1098/rspb.2011.0401)
  • Takasu, F., Why do all host species not show defence against avian brood parasitism: Evolutionary lag or equilibrium? (2010) Am. Nat, 151, pp. 193-205. , (doi:10.1086/286111)
  • Lotem, A., Nakamura, H., Evolutionary equilibria in avian brood parasitism: An alternative to the 'arms race-evolutionary lag' concept (1998) Parasitic birds and their hosts: Studies in coevolution, pp. 223-235. , In, (eds S. I. Rothstein & S. K. Robinson), Oxford, UK: Oxford University Press
  • Kruger, O., Cuckoos, cowbirds and hosts: Adaptations, trade-offs and constraints (2007) Phil. Trans. R. Soc. B, 362, pp. 1873-1886. , (doi:10.1098/rstb.2006.1849)
  • Rohwer, S., Spaw, C.D., Roskaft, E., Costs to Northern orioles of puncture-ejecting parasitic cowbird eggs from their nests (1989) Auk, 106, pp. 734-738
  • Roskaft, E., Rohwer, S., Spaw, C.D., Cost of puncture ejection compared with costs of rearing cowbird chicks for northern orioles (1993) Ornis Scand, 24, pp. 28-32. , (doi:10.2307/3676406)
  • Lotem, A., Nakamura, H., Zahavi, A., Constraints on egg discrimination and cuckoo host coevolution (1995) Anim. Behav, 49, pp. 1185-1209. , (doi:10.1006/anbe.1995. 0152)
  • Davies, N.B., Brooke, M.D., Kacelnik, A., Recognition errors and probability of parasitism determine whether reed warblers should accept or reject mimetic cuckoo eggs (1996) Proc. R. Soc. Lond. B, 263, pp. 925-931. , (doi:10.1098/rspb.1996.0137)
  • Kruger, O., Brood parasitism selects for no defence in a cuckoo host (2011) Proc. R. Soc. B, 278, pp. 2777-2783. , (doi:10.1098/rspb.2010.2629)
  • Soler, M., Soler, J.J., Martinez, J.G., Moller, A.P., Magpie host manipulation by great spotted cuckoos: Evidence for an avian Mafia? (1995) Evolution, 49, pp. 770-775. , (doi:10.2307/2410329)
  • Hoover, J., Robinson, S., Retaliatory mafia behavior by a parasitic cowbird favors host acceptance of parasitic eggs (2007) Proc. Natl Acad. Sci. USA, 104, pp. 4479-4483. , (doi:10.1073/pnas.0609710104)
  • Sato, N.J., Mikamf, O.K., Ueda, K., The egg dilution effect hypothesis: A condition under which parasitic nestling ejection behaviour will evolve (2010) Ornithol. Sci, 9, pp. 115-121. , (doi:10.2326/osj.9.115)
  • Davies, N.B., (2000) Cuckoos, cowbirds and other cheats., , London, UK: Princeton University Press
  • Rothstein, S.I., An experimental and teleonomic investigation of avian brood parasitism (1975) Condor, 77, pp. 250-271. , (doi:10.2307/1366221)
  • Davies, N.B., Brooke, M.L., An experimental study of co-evolution between the cuckoo, Cuculus canorus, and its hosts II. Host egg markings, chick discrimination and general discussion (1989) J. Anim. Ecol, 58, pp. 225-236. , (doi:10.2307/4996)
  • Marchetti, K., Costs to host defence and the persistence of parasitic cuckoos (1992) Proc. R. Soc. Lond. B, 248, pp. 41-45. , (doi:10.1098/rspb.1992.0040)
  • Takasu, F., Kawasaki, K., Nakamura, H., Cohen, J., Shigesada, N., Modeling the population dynamics of the cuckoo-host association and the evolution of host defences (1993) Am. Nat, 142, pp. 819-839. , (doi:10.1086/285574)
  • de Marsico, M., Mahler, B., Chomnalez, M., Di Giacomo, A., Reboreda, J., Host use by generalist and specialist brood parasitic cowbirds at population and individual levels (2010) Adv. Stud. Behav, 42, pp. 81-119. , (doi:10. 1016/S0065-3454(10)42003-3)
  • Fraga, R.M., Host-parasite interactions between chalk-browed mockingbirds and shiny cowbirds (1985) Ornithol. Monogr, 36, pp. 829-844
  • Mason, P., Brood parasitism in a host generalist the shiny cowbird Molothrus bonariensis II. Host selection (1986) Auk, 103, pp. 61-69
  • Sackmann, P., Reboreda, J.C., A comparative study of shiny cowbird parasitism of two large hosts, the chalk-browed mockingbird and the rufous-bellied thrush (2003) Condor, 105, pp. 728-736. , (doi:10.1650/7194)
  • Fiorini, V., (2007) Synchronization of parasitism and host selection in a generalist brood parasite, the shiny cowbird. Molothrus bonariensis, , (Icterinae, Aves). PhD thesis, University of Buenos Aires, Argentina
  • Salvador, S.A., Study of parasitism in raising shiny cowbirds Molothrus bonariensis and chalk-browed mockingbirds Mimus saturninus in Villa Maria Cordoba, Argentina (1984) Hornero, 12, pp. 141-149
  • Fiorini, V.D., Tuero, D.T., Reboreda, J.C., Shiny cowbirds synchronize parasitism with host laying and puncture host eggs according to host characteristics (2009) Anim. Behav, 77, pp. 561-568. , (doi:10.1016/j.anbehav.2008.11.025)
  • Snedecor, G.W., Cochran, W.G., (1989) Statistical methods, pp. 75-79. , 8th edn. Ames, IA: Blackwell Publishing
  • Peeters, E.H.M., Gardeniers, J.J.P., Logistic regression as a tool for defining habitat requirements of two common gammarids (1998) Freshwat. Biol, 39, pp. 605-615. , (doi:10.1046/j.1365-2427.1998.00304.x)
  • Llambías, P.E., Ferretti, V., Reboreda, J.C., Egg discrimination and sex-specific pecking behaviour in parasitic cowbirds (2006) Ethology, 112, pp. 1128-1135. , (doi:10. 1111/j.1439-0310.2006.01272.x)
  • Spaw, C.D., Rohwer, S., A comparative study of eggshell thickness in cowbirds and other passerines (1987) Condor, 89, pp. 307-318. , (doi:10.2307/1368483)
  • Picman, J., Mechanism of increased puncture resistance of eggs of brown-headed cowbirds (1989) Auk, 106, pp. 577-583
  • Brooker, M.G., Brooker, L.C., Eggshell strength in cuckoos and cowbirds (1991) Ibis, 133, pp. 406-413. , (doi:10. 1111/j.1474-919X.1991.tb04589.x)
  • Mermoz, M.E., Ornelas, J.F., Phylogenetic analysis of life-history adaptations in parasitic cowbirds (2004) Behav. Ecol, 15, pp. 109-119. , (doi:10.1093/beheco/arg102)
  • Rahn, H., Curran-Everett, L., Booth, D.T., Eggshell differences between parasitic and nonparasitic Icteridae (1988) Condor, 90, pp. 962-964. , (doi:10.2307/1368865)
  • Igic, B., Braganza, K., Hyland, M.M., Silyn-Roberts, H., Cassey, P., Grim, T., Rutila, J., Hauber, M.E., Alternative mechanisms of increased eggshell hardness of avian brood parasites relative to host species (2011) J. R. Soc. Interface, 8, pp. 1654-1664. , (doi:10.1098/rsif.2011.0207)
  • Zar, J.H., (1999) Biostatistical analysis, pp. 732-738. , 4th edn. London, UK: Prentice-Hall
  • Sealy, S.G., Evolution of host defences against brood parasitism: Implications of puncture-ejection by a small passerine (1996) Auk, 113, pp. 346-355
  • Peer, B.D., Sealy, S.G., Responses of scissortailed flycatchers (Tyrannus forficatus) to experimental cowbird parasitism (2000) Bird Behav, 13, pp. 63-67
  • Aviles, J.M., Soler, J.J., Soler, M., Moller, A.P., Rejection of parasitic eggs in relation to egg appearance in magpies (2004) Anim. Behav, 67, pp. 951-958. , (doi:10.1016/j. anbehav.2003.08.022)
  • Antonov, A., Stokke, B.G., Moksnes, A., Roskaft, E., Getting rid of the cuckoo Cuculus canorus egg: Why do hosts delay rejection? (2008) Behav. Ecol, 19, pp. 100-107. , (doi:10.1093/beheco/arm102)
  • Arias de Reyna, L., Coevolution of the great spotted cuckoo and its hosts (1998) Parasitic birds and their hosts: Studies in coevolution, pp. 129-142. , In, (eds S. I. Rothstein & S. K. Robinson), Oxford, UK: Oxford University Press
  • Ortega, C.P., Ortega, C.P., (1998) Cowbirds and other parasites, , Tuscon, AZ: University of Arizona Press
  • Astie, A.A., Reboreda, J., Costs of egg punctures and parasitism by shiny cowbirds (Molothrus bonariensis) at creamy-bellied thrush (Turdus amaurochalinus) nests (2006) Auk, 123, pp. 23-32. , (doi:10.1642/0004-8038(2006)123 [0023:COEPAP]2.0.CO;2)
  • Trivers, R.L., Parent-offspring conflict (1974) Am. Zool, 14, pp. 249-264. , (doi:10.1093/icb/14.1.249)
  • Hoover, J.P., Multiple effects of brood parasitism reduce the reproductive success of prothonotary warblers, Protonotaria citrea (2003) Anim. Behav, 65, pp. 923-934. , (doi:10.1006/anbe.2003.2155)
  • Hauber, M.E., Egg-capping is a cost paid by hosts of interspecific brood parasites (2003) Auk, 120, pp. 860-865. , (doi:10.1642/0004-8038(2003)120[0860:EI ACPB]2.0.CO;2)
  • Kilner, R.M., How selfish is a cowbird nestling? (2003) Anim. Behav, 66, pp. 569-576. , (doi:10.1006/anbe.2003.2204)
  • Fraga, R.M., Interactions of the parasitic screaming and shiny cowbirds (Molothrus rufoaxillaris and M. bonariensis) with a shared host, the bay-winged cowbird (M. badius) (1998) Parasitic birds and their hosts: Studies in coevolution, pp. 173-193. , In, (eds S. I. Rothstein & S. K. Robinson), Oxford, UK: Oxford University Press
  • Canestrari, D., Marcos, J.M., Baglione, V., Cooperative breeding in carrion crows reduces the rate of brood parasitism by great spotted cuckoos (2009) Anim. Behav, 77, pp. 1337-1344. , (doi:10.1016/j.anbehav.2009.02.009)
  • Gloag, R., Tuero, D.T., Fiorini, V.D., Reboreda, J.C., Kacelnik, A., The economics of nestmate-killing in avian brood parasites: A provisions trade-off (2011) Behav. Ecol, , (doi:10.1093/beheco/arr166)
  • Trivers, R.L., Parental investment and sexual selection (1972) Sexual selection and the descent of man, pp. 136-179. , In, (ed. B. Campbell), Chicago, IL: Aldine
  • Smith, J.N.M., Cowbird parasitism, host fitness, and age of the host female in an island song sparrow population (1981) Condor, 83, pp. 152-161. , (doi:10.2307/1367420)
  • Payne, R.B., Payne, L.L., Brood parasitism by cowbirds: Risks and effects on reproductive success and survival in indigo buntings (1998) Behav. Ecol, 9, pp. 64-73. , (doi:10.1093/beheco/9.1.64)
  • Sedgwick, J.A., Iko, W.M., Costs of brownheaded cowbird parasitism to willow flycatchers (1999) Stud. Avian Biol, 18, pp. 167-181
  • Mason, P., Rothstein, S.I., Crypsis versus mimicry and the color of shiny cowbird eggs (1987) Am. Nat, 130, pp. 161-167. , (doi:10.1086/284703)


---------- APA ----------
Gloag, R., Fiorini, V.D., Reboreda, J.C. & Kacelnik, A. (2012) . Brood parasite eggs enhance egg survivorship in a multiply parasitized host. Proceedings of the Royal Society B: Biological Sciences, 279(1734), 1831-1839.
---------- CHICAGO ----------
Gloag, R., Fiorini, V.D., Reboreda, J.C., Kacelnik, A. "Brood parasite eggs enhance egg survivorship in a multiply parasitized host" . Proceedings of the Royal Society B: Biological Sciences 279, no. 1734 (2012) : 1831-1839.
---------- MLA ----------
Gloag, R., Fiorini, V.D., Reboreda, J.C., Kacelnik, A. "Brood parasite eggs enhance egg survivorship in a multiply parasitized host" . Proceedings of the Royal Society B: Biological Sciences, vol. 279, no. 1734, 2012, pp. 1831-1839.
---------- VANCOUVER ----------
Gloag, R., Fiorini, V.D., Reboreda, J.C., Kacelnik, A. Brood parasite eggs enhance egg survivorship in a multiply parasitized host. Proc. R. Soc. B Biol. Sci. 2012;279(1734):1831-1839.