Skip to main content
SpringerLink
Log in

Multiple mechanisms of egg recognition in a cuckoo host

  • Original Article
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

The cognitive mechanisms behind egg rejection behavior have received increasing attention in recent years helping to understand the evolution of anti-parasite behavior by hosts. Here, we tested egg discrimination mechanisms of yellow-bellied prinia (Prinia flaviventris) in relation to different stages of egg laying (pre-egg laying, one host egg, and multi-host egg stages) and different extent of foreign egg mimicry (poor and high mimicry). We found that the prinia showed variation in egg rejection not only toward foreign eggs differing in mimicry but also among different stages of egg laying and within the same stage of laying. Prinias rejected 100 % of poorly mimetic foreign eggs in the pre-egg-laying stage, and 78.9 and 100 % in the one-host-egg and multi-host-egg stages, respectively. In contrast, they only rejected 38 % of highly mimetic eggs during the pre-egg-laying stage and accepted all at other stages. Multiple mechanisms, including a memory-based template through inheritance or learning, onset of laying, and direct comparison, may have evolved in the yellow-bellied prinia. The mechanisms depend on the mimicry of foreign eggs and the egg-laying stages tested. Innate or long-term memory template from previous breeding attempts may also be used in egg discrimination by hosts while observational learning or experience enhancement is involved in template formation, in which the first laying eggs may play a key role. However, discrimination during the pre-egg-laying stage may be a response toward foreign objects rather than parasitic eggs in this host species. These findings highlight the complexity of the multiple cognitive mechanisms involved in anti-parasite behavior.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abernathy VE, Peer BD (2014) Intraclutch variation in egg appearance of brown-headed cowbird hosts. Auk 131:467–475

    Article  Google Scholar 

  • 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 33:366–370

    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 

  • Bán M, Moskát C, Barta Z, Hauber ME (2013) Simultaneous viewing of own and parasitic eggs in not required for egg rejection by a cuckoo host. Behav Ecol 24:1014–1021

    Article  Google Scholar 

  • Bártol I, Karcza Z, Moskát C, Røskaft E, Kisbenedek T (2002) Responses of greed reed warblers Acrocephalus arundinaceus to experimental brood parasitism: the effect of a cuckoo Cuculus canorus dummy and egg mimicry. J Avian Biol 33:420–425

    Article  Google Scholar 

  • Bateson M, Healy SD (2005) Comparative evaluation and its implications for mate choice. Trends Ecol Evol 20:659–664

    Article  PubMed  Google Scholar 

  • Croston R, Hauber ME (2014) Spectral tuning and perceptual differences do not explain the rejection of brood parasitic eggs by American robins (Turdus migratorius). Behav Ecol Sociobiol 68:351–362

    Article  Google Scholar 

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

    Google Scholar 

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

    Article  Google Scholar 

  • Feeney WE, Welbergen JA, Langmore NE (2014) Advances in the study of coevolution between avian brood parasites and their hosts. Annu Rev Ecol Evol S 45:227–246

    Article  Google Scholar 

  • Hanley D, Samas P, Heryan 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. Sci Rep 5:9060

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hauber ME, Sherman PW (2001) Self-referent phenotype matching: theoretical considerations and empirical evidence. Trends Neurosci 24:609–616

    Article  CAS  PubMed  Google Scholar 

  • Hauber ME, Moskát C, Bán M (2006) Experimental shift in hosts’ acceptance threshold of inaccurate-mimic brood parasite eggs. Biol Lett 2:177–189

    Article  PubMed Central  PubMed  Google Scholar 

  • Holen ØH, Johnstone RA (2006) Context-dependent discrimination and the evolution of mimicry. Am Nat 167:377–389

    Article  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Langmore NE, Kilner RM, Butchart SHM, Maurer G, Davies NB, Cockburn A, Macgregor N, Peters A, Magrath MJL, Dowling D (2005) The evolution of egg rejection by cuckoo hosts in Australia and Europe. Behav Ecol 16:686–692

    Article  Google Scholar 

  • Liebert AE, Starks PT (2004) The action component of recognition systems: a focus on the response. Ann Zool Fenn 41:747–764

    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 

  • Marchetti K (2000) Egg rejection in a passerine bird: size does matter. Anim Behav 59:877–883

    Article  PubMed  Google Scholar 

  • Martín-Gálvez D, Soler JJ, Martínez JG, Krupa AP, Richard M, Soler M, Møller AP, Burke T (2006) A quantitative trait locus for recognition of foreign eggs in the host of a brood parasite. J Evol Biol 19:543–550

    Article  PubMed  Google Scholar 

  • Mateo JM (2004) Recognition systems and biological organization: the perception component of social recognition. Ann Zool Fenn 41:729–745

    Google Scholar 

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

    Article  Google Scholar 

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

    Google Scholar 

  • Molina-Morales M, Martínez JG, Martín-Gálvez D, Dawson DA, Burke T, Avilés JM (2014) Cuckoo hosts shift from accepting to rejecting parasitic eggs across their lifetime. Evolution 68:3020–3029

    Article  PubMed  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, Honza M (2002) European cuckoo Cuculus canorus parasitism and host’s rejection behaviour in a heavily parasitized great reed warbler Acrocephalus arundinaceus population. Ibis 144:614–622

    Article  Google Scholar 

  • Moskát C, Székely T, Kisbenedek T, Karcza Z, Bártol I (2003) The importance of nest cleaning in egg rejection behaviour of great reed warblers Acrocephalus arundinaceus. J Avian Biol 34:16–19

    Article  Google Scholar 

  • Moskát C, Bán M, Székely T, Komdeur J, Lucassen RW, van Boheemen LA, 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, Bán M, Hauber ME (2014a) Naïve hosts of avian brood parasites accept foreign eggs, whereas older hosts fine-tune foreign egg discrimination during laying. Front Zool 11:45

    Article  PubMed Central  PubMed  Google Scholar 

  • Moskát C, Hauber ME, Elek Z, Gommers M, Bán M, Groenewoud F (2014b) Foreign egg retention by avian hosts in repeated brood parasitism: why do rejecters accept? Behav Ecol Sociobiol 68:403–413

    Article  Google Scholar 

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

    Article  PubMed  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) An experimental and teleonomic investigation of avian brood parasitism. Condor 77:250–271

    Article  Google Scholar 

  • Rothstein SI, Robinson SK (1998) Parasitic birds and their hosts: studies in coevolution. Oxford University Press, Oxford

    Google Scholar 

  • Servedio MR, Hauber ME (2006) To eject or to abandon? Life history traits of hosts and parasites interact to influence the fitness payoffs of alternative anti-parasite strategies. J Evol Biol 19:1585–1594

    Article  CAS  PubMed  Google Scholar 

  • Servedio MR, Lande R (2003) Coevolution of an avian host and its parasitic cuckoo. Evolution 57:1164–1175

    Article  PubMed  Google Scholar 

  • Soler M (2014) Long-term coevolution between avian brood parasites and their hosts. Biol Rev 89:688–704

    Article  PubMed  Google Scholar 

  • Stokke BG, Rudolfsen G, Moksnes A, Røskaft E (2004) Rejection of conspecific eggs in chaffinches: the effect of age and clutch characteristics. Ethology 110:459–470

    Article  Google Scholar 

  • Stokke BG, Moksnes A, Røskaft E (2005) The enigma of imperfect adaptations in hosts of avian brood parasites. Ornithol Sci 4:17–29

    Article  Google Scholar 

  • Yang C, Møller AP, Røskaft E, Moksnes A, Liang W, Stokke BG (2014a) Reject the odd egg: egg recognition mechanisms in parrotbills. Behav Ecol 25:1320–1324

    Article  CAS  Google Scholar 

  • Yang C, Wang L, Cheng S-J, Hsu Y-C, Liang W, Moller AP (2014b) Nest defenses and egg recognition of yellow-bellied prinia against cuckoo parasitism. Naturwissenschaften 101:727–734

    Article  CAS  PubMed  Google Scholar 

  • Yang C, Wang L, Liang W, Møller AP (2015) Nest sanitation behavior in hirundines as a pre-adaptation to egg rejection to counter brood parasitism. Anim Cogn 18:355–360

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We would like to thank Ian Will, University of California, Berkeley, USA, Aiwu Jiang, Mingde Jiang, Qiuli Huang, and Yungao Hu for their assistance with the fieldwork. We thank Jianchou Nong and his family for help with the logistics. This work was supported by the National Natural Science Foundation of China (Nos. 31260514 to CY, 31272328 and 31472013 to WL) and Program for New Century Excellent Talents in University (NCET-13-0761) to CY.

Conflict of interest

The authors declare that they have no competing interests.

Ethical standards

The experiments comply with the current laws of China, where they were performed. Fieldwork was carried out under the permission of Nonggang National Nature Reserve, China. Experimental procedures were in agreement with the Animal Research Ethics Committee of Hainan Provincial Education Centre for Ecology and Environment, Hainan Normal University.

Author information

Authors and Affiliations

  1. College of Life Sciences, Wuhan University, Wuhan, 430072, China

    Longwu Wang & Xin Lu

  2. Ministry of Education Key Laboratory for Tropical Plant and Animal Ecology, College of Life Sciences, Hainan Normal University, Haikou, 571158, China

    Longwu Wang, Canchao Yang & Wei Liang

  3. Laboratoire d’Ecologie, Systématique et Evolution, CNRS UMR 8079, Université Paris-Sud, Bâtiment 362, F-91405, Orsay Cedex, France

    Anders P. Møller

Authors
  1. Longwu Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Canchao Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Anders P. Møller
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Wei Liang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xin Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Wei Liang or Xin Lu.

Additional information

Communicated by N. Clayton

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, L., Yang, C., Møller, A.P. et al. Multiple mechanisms of egg recognition in a cuckoo host. Behav Ecol Sociobiol 69, 1761–1767 (2015). https://doi.org/10.1007/s00265-015-1988-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-015-1988-8

Keywords

Search

Navigation