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Coots use hatch order to learn to recognize and reject conspecific brood parasitic chicks

Naturevolume 463, pages223–226 (2010)Cite this article

Abstract

Avian brood parasites and their hosts provide model systems for investigating links between recognition, learning, and their fitness consequences1,2,3,4. One major evolutionary puzzle has continued to capture the attention of naturalists for centuries: why do hosts of brood parasites generally fail to recognize parasitic offspring after they have hatched from the egg5,6,7,8,9, even when the host and parasitic chicks differ to almost comic degrees7? One prominent theory to explain this pattern proposes that the costs of mistakenly learning to recognize the wrong offspring make recognition maladaptive10. Here we show that American coots,Fulica americana, can recognize and reject parasitic chicks in their brood by using learned cues, despite the fact that the hosts and the brood parasites are of the same species. A series of chick cross-fostering experiments confirm that coots use first-hatched chicks in a brood as referents to learn to recognize their own chicks and then discriminate against later-hatched parasitic chicks in the same brood. When experimentally provided with the wrong reference chicks, coots can be induced to discriminate against their own offspring, confirming that the learning errors proposed by theory can exist10. However, learning based on hatching order is reliable in naturally parasitized coot nests because host eggs hatch predictably ahead of parasite eggs. Conversely, a lack of reliable information may help to explain why the evolution of chick recognition is not more common in hosts of most interspecific brood parasites.

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Figure 1:Chick survival at naturally parasitized broods.
Figure 2:Cross-fostering experiments to confirm chick recognition and its mechanism.
Figure 3:The hatch order mechanism for chick recognition.

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Acknowledgements

We thank J. Herrick and W. Messner for access to their property; B. Bair, L. Cargill, E. Clancey, J. Clark, J. Click, R. Drobek, S. Everding, K. Funk, J. Garcia, L. Hamilton, D. Hansen, E. Hoosier, M. Magrath, J. Melhaff, C. Morrill, C. Nelson, A. O’Brien, L. Orr, G. Peters, G. Taylor, K. Tjernell and J. Sapp for assistance in the field; B. Sinervo for advice on the study design; J. Eadie, A. Lotem, D. Mock, R. Montgomerie, R. Mulder, K. Wasson and A. Zink for helpful comments on the paper; and P. Raimondi and R. Montgomerie for statistical advice. Funding was provided by the National Geographic Society, the National Science Foundation (DDIG IOS-0808579 to D.S., and IOS 0443807 to B.E.L.), the Chapman Fund and the Sigma Xi Society. Fieldwork was conducted under permits from the Canadian Wildlife Service and the University of California, Santa Cruz, Institutional Animal Care and Use Committee.

Author Contributions D.S. designed the experiments, and developed the conceptual framework. D.S. and B.E.L. conducted the fieldwork and wrote the paper.

Author information

Authors and Affiliations

  1. Department of Ecology and Evolutionary Biology, University of California, Santa Cruz, California 95064, USA,

    Daizaburo Shizuka & Bruce E. Lyon

Authors
  1. Daizaburo Shizuka

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  2. Bruce E. Lyon

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Corresponding author

Correspondence toDaizaburo Shizuka.

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Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Notes, Supplementary Table 1, Supplementary Figure 1 with Legend and Supplementary References. (PDF 113 kb)

Supplementary Video 1

This movie shows a parent coot ‘touseling’ its chick, whereby the chick is grabbed by the nape and gently shaken. This form of parental aggression is common in coot broods to control food allocation, and differs from the forms of aggression associated with infanticidal chick rejection shown in the other movies. (MOV 3407 kb)

Supplementary Video 2

This movie shows infanticidal parental aggression by an adult male coot towards a natural brood parasitic chick in its brood (a non-experimental brood). (MOV 5797 kb)

Supplementary Video 3

This movie shows an adult female coot attacking an experimental foreign chick in a Host First experimental brood. During several hours of observation the female repeatedly attacked this same chick, often actively seeking it out. (MOV 5297 kb)

Supplementary Video 4

This movie shows parental aggression by an adult female coot towards its own chick in a Foreign First experimental brood. The aggression towards the chicks includes pecking, pulling the chick off a floating algal mat and holding the chick’s head in the water. (MOV 4301 kb)

Supplementary Video 5

This movie shows an adult female coot at a Foreign First Experimental nest pecking several chicks during a brooding session; all three of the chicks observed being pecked were the female’s own chicks. (MOV 5583 kb)

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Shizuka, D., Lyon, B. Coots use hatch order to learn to recognize and reject conspecific brood parasitic chicks.Nature463, 223–226 (2010). https://doi.org/10.1038/nature08655

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Editorial Summary

Best of the nest

Many birds that are targeted by brood parasites have learnt to reject the parasites' eggs, but very few reject parasite chicks if they manage to hatch, even though they can be absurdly different in size from their own chicks. A series of chick cross-fostering experiments in one of the rare cases where chick rejection does occur, parasitism within a species (American coots), shows that the parents use the first of their brood to hatch as a template against which to judge potential intruders hatching later. This learning rule may explain the puzzling absence of chick recognition as a host defence against avian brood parasites: it may be counterproductive for the hosts of most interspecific parasites as the intruder usually hatches early and would stand a good chance of becoming the brood template.

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