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Experimental evidence for an antipredatory function of egg rejection behaviour in a common host of the brood-parasitic shiny cowbird

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Abstract

The rejection of foreign eggs is the most effective adaptation against brood parasitism in birds. Many hosts, however, show suboptimal responses towards parasitic eggs, which could reflect a compromise between the benefits and costs of egg rejection. Some large-sized hosts of the shiny cowbird (Molothrus bonariensis) accept any spotted parasite egg but reject a rarer pure white egg morph that occurs only in some parts of the parasite’s distribution. This behaviour is intriguing because it is not an effective defence against parasitism and recent evidences suggest that large-sized hosts could benefit from accepting cowbird eggs as this may dilute the risk of host egg losses at multiply parasitized nests. We studied whether rejection of pure white cowbird eggs can be driven by the increased predation risk of host nests parasitized with this conspicuous egg morph. We conducted a nest predation experiment using artificial clutches placed in natural, inactive nests of a large-sized host, the chalk-browed mockingbird (Mimus saturninus). Clutches consisted of two eggs resembling either one host plus one pure white cowbird egg, one host plus one spotted cowbird egg or two host eggs. Clutches with pure white eggs were more likely to be predated than those having either two host eggs or one host and one spotted cowbird egg, supporting an antipredatory function of egg rejection behaviour in mockingbirds. These results suggest that nest predation could operate as part of larger fitness trade-offs shaping host responses towards foreign eggs. Considering the role of nest predation in the studies of host rejection decisions would help to better understand the evolution and expression of antiparasite defences, especially when the hosts seem to behave suboptimally against costly brood parasitism.

Significance statement

One major goal in avian brood parasitism research is to explain the evolution of host defences against parasite eggs and young. Some large-sized hosts of the shiny cowbird (Molothrus bonariensis) show an intriguing behaviour: they accept spotted cowbird eggs but reject a rare pure white egg morph that occurs only in some parts of the parasite’s distribution. Such behaviour provides little protection against parasitism, but it may serve as an antipredatory defence if conspicuous pure white eggs facilitate the detection of host nests to potential predators. Our study supports this idea by showing that pure white eggs increase the risk of nest predation compared to spotted host and cowbird eggs in a common large-sized host, the chalk-browed mockingbird (Mimus saturninus). These findings highlight the importance of considering the role of nest predation in the expression of hosts’ strategies against parasitism.

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References

  • Antonov A, Stokke BG, Moksnes A, Kleven O, Honza M, Røskaft E (2006) Eggshell strength of an obligate brood parasite: a test of the puncture resistance hypothesis. Behav Ecol Sociobiol 60:11–18

    Article  Google Scholar 

  • Antonov A, Stokke BG, Moksnes A, Røskaft E (2008) Getting rid of the cuckoo Cuculus canorus egg: why do hosts delay rejection? Behav Ecol 19:100–107

    Article  Google Scholar 

  • Astié AA, Reboreda JC (2005) Creamy-bellied thrush defenses against shiny cowbird parasitism. Condor 107:788–796

    Article  Google Scholar 

  • Astié AA, Reboreda JC (2006) Costs of egg punctures and parasitism by shiny cowbirds (Molothrus bonariensis) at creamy-bellied thrush (Turdus amaurochalinus) nests. Auk 123:23–32

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2014) “lme4: Linear mixed-effects models using Eigen and S4”. R package version 1.1–7, http://CRAN.R project.org/package=lme4

  • Brennan PL (2010) Clutch predation in great tinamous Tinamus major and implications for the evolution of egg color. J Avian Biol 41:419–426

    Article  Google Scholar 

  • Carro ME, Fernández GJ (2013) Can nest predation explain the lack of defenses against cowbird brood parasitism in the rufous-collared sparrow (Zonotrichia capensis)? Auk 130:408–416

    Article  Google Scholar 

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

    Google Scholar 

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

    Article  Google Scholar 

  • Davies NB, Brooke M d L (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 

  • Davies NB, Brooke M d L, Kacelnik A (1996) Recognition errors and probability of parasitism determine whether reed warblers should accept or reject mimetic cuckoo eggs. Proc R Soc Lond B 263:925–931

    Article  Google Scholar 

  • de la Colina MA, Pompilio 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 

  • 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 

  • Fraga RM (1985) Host-parasite interactions between chalk-browed mockingbirds and shiny cowbirds. Ornithol Monogr 36:828–844

    Google Scholar 

  • Gillis H, Gauffre B, Huot R, Bretagnolle V (2012) Vegetation height and egg coloration differentially affect predation rate and overheating risk: an experimental test mimicking a ground-nesting bird. Can J Zool 90:694–703

    Article  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 

  • Gloag R, Fiorini VD, Reboreda JC, Kacelnik A (2014) Shiny cowbirds share foster mothers but not true mothers in multiply parasitized mockingbird nests. Behav Ecol Sociobiol 68:681–689

    Article  Google Scholar 

  • Götmark F (1992) Blue eggs do not reduce nest predation in the song thrush, Turdus philomelos. Behav Ecol Sociobiol 30:245–252

    Article  Google Scholar 

  • Guigueno MF, Sealy SG (2009) Nest sanitation plays a role in egg burial by yellow warblers. Ethology 115:247–256

    Article  Google Scholar 

  • Hauber ME, Tong L, Bán M, Croston R, Grim T, Waterhouse GI, 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 121:521–528

    Article  Google Scholar 

  • Hoover JP, Robinson SK (2007) Retaliatory mafia behavior by a parasitic cowbird favors host acceptance of parasitic eggs. Proc Natl Acad Sci U S A 104:4479–4483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ibañez-Alamo JD, Soler M (2012) Predator-induced female behavior in the absence of male incubation feeding: an experimental study. Behav Ecol Sociobiol 66:1067–1073

    Article  Google Scholar 

  • Kilner RM (2006) The evolution of egg colour and patterning in birds. Biol Rev 81:383–406

    Article  CAS  PubMed  Google Scholar 

  • Krüger O (2011) Brood parasitism selects for no defence in a cuckoo host. Proc R Soc Lond B 278:2777–2783

    Article  Google Scholar 

  • Lahti DC (2015) The limits of artificial stimuli in behavioral research: the umwelt gamble. Ethology 121:529–537

    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 

  • Lichtenstein G (1998) Parasitism by shiny cowbirds of rufous-bellied thrushes. Condor 100:680–687

    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 

  • Lotem A, Nakamura H, Zahavi A (1995) Constraints on egg discrimination and cuckoo-host coevolution. Anim Behav 49:1185–1209

    Article  Google Scholar 

  • Marchetti K (1992) Costs to host defence and the persistence of parasitic cuckoos. Proc R Soc Lond B 248:41–45

    Article  CAS  Google Scholar 

  • Martin TE, Scott J, Menge C (2000) Nest predation increases with parental activity: separating nest site and parental activity effects. Proc R Soc Lond B 267:2287–2293

    Article  CAS  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 

  • Mason P, Rothstein SI (1987) Crypsis versus mimicry and the color of shiny cowbird eggs. Am Nat 130:161–167

    Article  Google Scholar 

  • Mermoz ME, Reboreda JC (1994) Brood parasitism of the shiny cowbird, Molothrus bonariensis, on the brown-and-yellow marshbird, Pseudoleistes virescens. Condor 96:716–721

    Article  Google Scholar 

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

    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 

  • Ortega CP (1998) Cowbirds and other brood parasites. University of Arizona Press, Tucson

    Google Scholar 

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

    Article  Google Scholar 

  • R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Viena http://www.R-project.org

    Google Scholar 

  • Røskaft E, Moksnes A (1998) Coevolution between brood parasites and their hosts: an optimality theory approach. In: Rothstein SI, Robinson SK (eds) Parasitic birds and their hosts: studies in coevolution. Oxford University Press, New York, pp. 236–254

    Google Scholar 

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

    Article  Google Scholar 

  • Røskaft E, Rohwer S, Spaw CD (1993) Cost of puncture ejection compared with costs of rearing cowbird chicks for northern orioles. Ornis Scand 24:28–32

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Salvador SA (1984) Estudio de parasitismo de cría del Renegrido (Molothrus bonariensis) en Calandria (Mimus saturninus), en Villa María, Córdoba. Hornero 12:141–149

    Google Scholar 

  • Sato NJ, Mikami OK, Ueda K (2010) The egg dilution effect hypothesis: a condition under which parasitic nestling ejection behaviour will evolve. Ornithol Sci 9:115–121

    Article  Google Scholar 

  • Sealy SG (1995) Burial of cowbird eggs by parasitized yellow warblers: an empirical and experimental study. Anim Behav 49:877–889

    Article  Google Scholar 

  • Singmann H, Bolker B, Westfall J (2015) afex: analysis of factorial experiments. R package version 0.15–2, https://CRAN.R-project.org/package=afex

  • Soler JJ, Sorci G, Soler M, Møller AP (1999) Change in host rejection behavior mediated by the predatory behavior of its brood parasite. Behav Ecol 10:275–280

    Article  Google Scholar 

  • Strausberger BM, Burhans DE (2001) Nest desertion by field sparrows and its possible influence on the evolution of cowbird behavior. Auk 118:770–776

    Article  Google Scholar 

  • 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 19:74–116

    Article  Google Scholar 

  • Tuero DT, Fiorini VD, Reboreda JC (2012) Do shiny cowbird females adjust egg pecking behavior according to the level of competition their chicks face in host nests? Behav Process 89:137–142

    Article  Google Scholar 

  • Underwood TJ, Sealy SG (2002) Adaptive significance of egg coloration. In: Deeming DC (ed) Avian incubation, behaviour, environment, and evolution. Oxford University Press, Oxford, pp. 280–298

    Google Scholar 

  • Weidinger K (2001) Does egg colour affect predation rate on open passerine nests? Behav Ecol Sociobiol 49:456–464

    Article  Google Scholar 

  • Weidinger K, Kočvara R (2010) Repeatability of nest predation in passerines depends on predator species and time scale. Oikos 119:138–146

    Article  Google Scholar 

  • Westmoreland D (2008) Evidence of selection for egg crypsis in conspicuous nests. J Field Ornithol 79:263–268

    Article  Google Scholar 

  • Westmoreland D, Best LB (1986) Incubation continuity and the advantage of cryptic egg coloration to mourning doves. Wilson Bull 98:297–300

    Google Scholar 

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Acknowledgments

We thank Fundación Elsa Shaw de Pearson for allowing us to conduct this study at ‘Reserva El Destino’ and F. Lama for assistance in the field. We are also grateful to M. A. de la Colina who generously provided us the reflectance spectra of natural eggs and B. Mahler and four anonymous referees for providing helpful comments on the earlier drafts of this manuscript. MCDM and JCR are fellows from Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) and CAU has a scholarship from CONICET. This work was supported by research grants from the University of Buenos Aires (W808) and Agencia Nacional de Promoción Científica y Tecnológica (PICT-2011-0045).

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

    María C. De Mársico, Cynthia A. Ursino & Juan C. Reboreda

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  1. María C. De Mársico
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  2. Cynthia A. Ursino
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  3. Juan C. Reboreda
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Correspondence to María C. De Mársico.

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The study was founded by research grants from the University of Buenos Aires (W808) and Agencia Nacional de Promoción Científica y Tecnológica (PICT-2011-0045).

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The authors declare that they have no conflict of interest.

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This article does not contain any studies with human participants or animals performed by any of the authors.

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Communicated by M. Soler

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De Mársico, M.C., Ursino, C.A. & Reboreda, J.C. Experimental evidence for an antipredatory function of egg rejection behaviour in a common host of the brood-parasitic shiny cowbird. Behav Ecol Sociobiol 70, 1689–1697 (2016). https://doi.org/10.1007/s00265-016-2174-3

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