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Foreign egg retention by avian hosts in repeated brood parasitism: why do rejecters accept?

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Abstract

Great reed warblers (Acrocephalus arundinaceus) are frequently parasitized by egg-mimetic common cuckoos (Cuculus canorus) in Hungary, and these hosts reject about a third of parasitic eggs. The timing of parasitism is important, in that the probability of rejection decreases with advancing breeding stages in this host. Also, egg rejection is more common when a clutch is parasitized by a single foreign egg, compared to parasitism by multiple eggs. We repeatedly parasitized great reed warbler clutches with moderately mimetic foreign eggs, either with (1) one foreign egg (single parasitism) and, after 3 days, by all foreign eggs (multiple parasitism), or (2) all foreign eggs and, 3 days later, by only one foreign egg. Hosts ejected 26–53 % of the experimental parasitic eggs in the first stage of the repeated parasitism, but almost all eggs were accepted in the second stage, irrespective of whether the clutch was singly or multiply parasitized. Video-taping of the behavioural responses of hosts to experimental parasitism revealed no evidence for sensory constraints on foreign-egg recognition, because hosts recognized and pecked the parasitic eggs as frequently in the second stage of repeated parasitism, as they did in the first stage. We suggest that the relative timing of parasitism (laying vs. incubation stage), rather than learning to accept earlier-laid foreign eggs, results in higher acceptance rates of cuckoo eggs in repeated parasitism, because there is decreasing natural cuckoo parasitism on this host species and, hence, less need for antiparasitic defences, with the advancing stages of breeding.

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References

  • Anderson MG, Moskát C, Bán M, Grim T, Cassey P, Hauber MA (2009) Egg eviction imposes a recoverable cost of virulence in chicks of a brood parasite. PLoS ONE 4:e7725

    Article  PubMed Central  PubMed  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 

  • 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 

  • Antonov A, Stokke BG, Vikan JR, Fossøy F, Ranke PS, Røskaft E, Moksnes A, Møller AP, Shykoff JA (2010) Egg phenotype differentiation in sympatric cuckoo Cuculus canorus gentes. J Evol Biol 23:1170–1182

    Article  PubMed  Google Scholar 

  • Avilés JM (2008) Egg colour mimicry in the common cuckoo Cuculus canorus as revealed by modelling host retinal function. Proc R Soc Lond B 275:2345–2352

    Article  Google Scholar 

  • Bán M, Barta Z, Munoz AR, Takasu F, Nakamura H, Moskát C (2011) The analysis of common cuckoo's egg shape in relation to its hosts' in two geographically distant areas. J Zool 284:77–83

    Article  Google Scholar 

  • 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 24:1014–1021

    Article  Google Scholar 

  • Begum S, Moksnes A, Røskaft E, Stokke BG (2012) Responses of potential hosts of Asian cuckoos to experimental parasitism. Ibis 154:363–371

    Article  Google Scholar 

  • Birkhead TR, Hemmings N, Spottiswoode CN, Mikulica O, Moskát C, Bán M, Schulze-Hagen K (2011) Internal incubation and early hatching in brood parasitic birds. Proc R Soc Lond B 278:1019–1024

    Article  CAS  Google Scholar 

  • Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White J-SS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135

    Article  PubMed  Google Scholar 

  • Box G (1988) Signal-to-noise ratios, performance criteria, and transformations. Technometrics 30:1–17

    Article  Google Scholar 

  • Brooke MdeL, Davies NB (1988) Egg mimicry by cuckoos Cuculus canorus in relation to discrimination by hosts. Nature 335:630–632

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Clutton-Brock TH (1991) The evolution of parental care. Princeton University Press, Princeton

    Google Scholar 

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

    Google Scholar 

  • Davies NB (2011) Cuckoo adaptations: trickery and tuning. J Zool 284:1–14

    Article  Google Scholar 

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

    Google Scholar 

  • Davies NB, Brooke MdeL (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

    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 

  • Geltsch N, Hauber ME, Anderson MG, Bán M, Moskát C (2012) Competition with a host nestling for parental provisioning imposes recoverable costs on parasitic cuckoo chick’s growth. Behav Process 90:378–383

    Article  Google Scholar 

  • Grim T (2002) Why is mimicry in cuckoo eggs sometimes so poor? J Avian Biol 33:302–305

    Article  Google Scholar 

  • Grim T, Samas 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

    Article  PubMed  Google Scholar 

  • Hale K, Briskie JV (2007) Response of introduced European birds in New Zealand to experimental brood parasitism. J Avian Biol 38:198–204

    Article  Google Scholar 

  • Hargitai R, Moskát C, Bán M, Gil D, López-Rull I, Solymos E (2010) Eggshell characteristics and yolk composition in the common cuckoo Cuculus canorus: are they adapted to brood parasitism? J Avian Biol 41:177–185

    Article  Google Scholar 

  • Hauber ME, Moskát C (2008) Shared parental care is costly for nestlings of common cuckoos and their great reed warbler hosts. Behav Ecol 19:79–86

    Article  Google Scholar 

  • Hauber ME, Yeh PJ, Roberts JOL (2004) Patterns and coevolutionary consequences of repeated brood parasitism. Proc R Soc Lond B 271:S317–S320

    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

    Article  PubMed Central  PubMed  Google Scholar 

  • Higuchi H (1998) Host use and egg color of Japanese cuckoos. In: Rothstein SI, Robinson SK (eds) Parasitic birds and their hosts. Studies in coevolution. Oxford University Press, New York, pp 80–93

    Google Scholar 

  • Honza M, Pozgayová M, Procházka P, Kadlec E (2007) Consistency in egg rejection behaviour: responses to repeated brood parasitism in the blackcap (Sylvia atricapilla). Ethology 113:344–351

    Article  Google Scholar 

  • Honza M, Procházka P, Pozgayová M (2012) Within- and between-season repeatability of eggshell colouration in the great reed warbler Acrocephalus arundinaceus. J Avian Biol 43:91–96

    Article  Google Scholar 

  • 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 76:1208–1214

    Article  PubMed  Google Scholar 

  • Hoover JP, Yasukawa K, Hauber ME (2006) Spatially and temporally structured avian brood parasitism affects the fitness benefits of hosts’ rejection strategies. Anim Behav 72:881–890

    Article  Google Scholar 

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

    Article  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 colour mimicry. Proc R Soc Lond B 279:1068–1076

    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 

  • 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, Lahti AR (2002) How precise is egg discrimination in weaverbirds? Anim Behav 63:1135–1142

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Lyon B (2003) Egg recognition and counting reduce costs of avian conspecific brood parasitism. Nature 422:495–499

    Article  CAS  PubMed  Google Scholar 

  • Moksnes A (1992) Egg recognition in chaffinches and bramblings. Anim Behav 44:993–995

    Article  Google Scholar 

  • Moksnes A, Røskaft E (1995) Egg-morph and host preferences 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 

  • Moksnes A, Røskaft E, Braa AT, Korsnes L, Lampe HM, Pedersen HC (1991) Behavioural responses of potential hosts towards artificial cuckoo eggs and dummies. Behaviour 116:64–89

    Article  Google Scholar 

  • Molina-Morales M, Martínez JG, Martín-Gálvez D, Dawson DA, Rodríguez-Ruiz J, Burke T, Avilés JA (2012) Evidence of long-term structured cuckoo parasitism on individual magpie hosts. J Anim Ecol 42:579–580

    Google Scholar 

  • Molnár B (1939) About the cuckoo. Observations and experiments on the eviction instinct of the cuckoo chick. Published by the author, Szarvas, Hungary (In Hungarian)

  • Moskát C (2005) Nest defence and egg rejection in great reed warblers over the breeding cycle: are they synchronised with the risk of brood parasitism? Ann Zool Fenn 42:579–586

    Google Scholar 

  • Moskát C, Fuisz TI (1999) Reactions of red-backed shrikes Lanius collurio to artificial cuckoo Cuculus canorus eggs. J Avian Biol 30:175–181

    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, Hauber ME (2010) Chick loss from mixed broods reflects severe nestmate competition between an evictor brood parasite and its hosts. Behav Process 83:311–314

    Article  Google Scholar 

  • Moskát C, Hauber ME, Avilés JA, Bán M, Hargitai R, Honza M (2009) Increased host tolerance of multiple cuckoo eggs leads to higher fledging success of the brood parasite. Anim Behav 77:1281–1990

    Article  Google Scholar 

  • Moskát C, Bán M, Székely T, Komdeur J, Lucassen RWG, van Boheemen AL, 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 

  • Moskát C, Takasu F, Munoz AR, Nakamura H, Bán M, Barta Z (2012) Cuckoo parasitism on two closely-related Acrocephalus warblers in distant areas: a case of parallel coevolution? Chin Birds 3:320–329

    Article  Google Scholar 

  • Nakagawa S, Hauber ME (2011) Great challenges with few subjects: statistical strategies for neuroscientists. Neurosci Biobehav Rev 35:462–473

    Article  PubMed  Google Scholar 

  • Peer BD, Rothstein SI (2010) Phenotypic plasticity in common grackles (Quiscalus quiscula) in response to repeated brood parasitism. Auk 127:293–299

    Article  Google Scholar 

  • Pinheiro J, Bates D, DebRoy S, Sarkar D and the R Development Core Team (2012) nlme: linear and nonlinear mixed effects models. R package version 3.1-106 URL http://CRAN.R-project.org/package=nlme

  • Polaciková L, Takasu F, Stokke BG, Moksnes A, Røskaft E, Cassey P, Hauber ME, Grim T (2013) Egg arrangement in avian clutches covaries with the rejection of foreign eggs. Anim Cogn 16:819–828

    Article  PubMed  Google Scholar 

  • Pozgayová M, Procházka M, Honza M (2009) Sex-specific defence behaviour against brood parasitism in a host with female-only incubation. Behav Process 81:34–38

    Article  Google Scholar 

  • Pozgayová M, Procházka M, Polaciková L, Honza M (2011) Closer clutch inspection — quicker egg ejection: timing of host responses toward parasitic eggs. Behav Ecol 22:46–51

    Article  Google Scholar 

  • R Core Team (2012) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://www.R-project.org/

  • Rensch B (1925) Verhalten von Singvogeln bei Aenderung des Geleges. Ornithol Monatschr 33:16–173

    Google Scholar 

  • Rodríguez-Gironés MA, Lotem A (1999) How to detect a cuckoo egg: a signal-detection theory model for recognition and learning. Am Nat 153:633–648

    Article  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 

  • Rothstein SI (1974) Mechanisms of avian egg recognition: possible learned and innate factors. Auk 91:796–807

    Article  Google Scholar 

  • Rothstein SI (1975) Mechanisms of avian egg recognition: do birds know their own eggs? Anim Behav 23:268–278

    Article  Google Scholar 

  • Rothstein SI (1976) Experiments on defenses cedar waxwings use against cowbird parasitism. Auk 93:675–691

    Google Scholar 

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

    Article  Google Scholar 

  • Sealy SG, Underwood TJ (2012) Egg discrimination by hosts and obligate brood parasites: a historical perspective and new synthesis. Chin Birds 3:274–294

    Article  Google Scholar 

  • Soler M, Martín-Vivaldi M, Pérez-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 108:1093–1101

    Article  Google Scholar 

  • Soler M, Fernández-Morante J, Espinoza F, Martin-Vivaldi M (2012a) Pecking but accepting the parasitic eggs may not reflect ejection failure: the role of motivation. Ethology 118:1–11

    Article  Google Scholar 

  • Soler M, Martín-Vivaldi M, Fernández-Morante J (2012b) Conditional response by hosts to parasitic eggs: the extreme case of the rufous-tailed scrub robin. Anim Behav 84:421–426

    Article  Google Scholar 

  • Soler M, Ruiz-Castellano C, Carra LG, Ontanilla J, Martín-Galvez D (2013) Do first-time breeding females imprint on their own eggs? Proc R Soc Lond B 280:20122518

    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 

  • Stokke BG, Honza M, Moksnes A, Røskaft E, Rudolfsen G (2002) Costs associated with recognition and rejection of parasitic eggs in two European passerines. Behaviour 139:629–644

    Article  Google Scholar 

  • Stokke BG, Takasu F, Moksnes A, Røskaft E (2007) The importance of clutch characteristics and learning for antiparasite adaptations in hosts of avian brood parasites. Evolution 61:2212–2228

    Article  PubMed  Google Scholar 

  • Strausberger BM, Rothstein SI (2009) Parasitic cowbirds may defeat host defense by causing rejecters to misimprint on cowbird eggs. Behav Ecol 20:691–699

    Article  Google Scholar 

  • Trnka A, Pozgayová M, Procházka P, Prokop P, Honza M (2012) Breeding success of a brood parasite is associated with social mating status of its host. Behav Ecol Sociobiol 66:1187–1194

    Article  Google Scholar 

  • Underwood TJ, Sealy SG (2006) Parameters of brown-headed cowbird Molothrus ater egg discrimination in warbling vireos Vireo gilvus. J Avian Biol 37:457–466

    Article  Google Scholar 

  • Wheelwright NT, Graff ES, Norris DR (2012) Relative consistency in size, shape, and coloration of savannah sparrow eggs within and between breeding seasons. Condor 114:412–420

    Article  Google Scholar 

  • Zeleis A, Hothorn T (2002) Diagnostic checking in regression relationships. R News 2:7–10 URL http://CRAN.R-project.org/doc/Rnews/

    Google Scholar 

  • Zölei A, Hauber ME, Geltsch N, Moskát C (2012) Asymmetrical signal content of egg shape as predictor of egg rejection by great reed warblers, hosts of the common cuckoo. Behaviour 149:391–406

    Article  Google Scholar 

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Acknowledgments

The Hungarian National Science Fund (OTKA, No. 83217 to CM) supported the study. For additional funding, we thank the Human Frontier Science Program and PSC-CUNY (to MEH). István Zsoldos, Nikoletta Geltsch, and Anikó Zölei kindly helped us during the field work.

Ethical standards

The Middle- and Lower-Danube-Valley Inspectorates for Environmental Protection, Nature Conservation and Water Management provided permission for research. The authors declare that their experiments performed in this study comply with the laws of Hungary.

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Authors and Affiliations

  1. MTA-ELTE-MTM Ecology Research Group, Hungarian Academy of Sciences, c/o Biological Institute, Eötvös Lóránd University and Hungarian Natural History Museum, Pázmány Péter sétány 1/C., Budapest, H-1117, Hungary

    Csaba Moskát & Zoltán Elek

  2. Department of Psychology, Hunter College and the Graduate Center of the City University of New York, 695 Park Avenue, New York, NY, 10065, USA

    Márk E. Hauber

  3. Behavioural Ecology and Self-organization, Centre for Ecological and Evolutionary Studies, University of Groningen, P.O. Box 11103, 9700 CC, Groningen, The Netherlands

    Moniek Gommers, Frank Groenewoud, Tom S. L. Versluijs, Christiaan W. A. Hoetz & Jan Komdeur

  4. MTA-DE “Lendület” Behavioural Ecology Research Group, Department of Evolutionary Zoology, University of Debrecen, Debrecen, 4010, Hungary

    Miklós Bán

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  1. Csaba Moskát
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  2. Márk E. Hauber
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  3. Zoltán Elek
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  4. Moniek Gommers
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  6. Frank Groenewoud
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  7. Tom S. L. Versluijs
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  8. Christiaan W. A. Hoetz
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  9. Jan Komdeur
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Correspondence to Csaba Moskát.

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Communicated by M. Soler

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Moskát, C., Hauber, M.E., Elek, Z. et al. Foreign egg retention by avian hosts in repeated brood parasitism: why do rejecters accept?. Behav Ecol Sociobiol 68, 403–413 (2014). https://doi.org/10.1007/s00265-013-1654-y

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