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

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.

References

  1. 1

    Rothstein, S. I. A model system for coevolution—avian brood parasitism. Annu. Rev. Ecol. Syst. 21, 481–508 (1990)

    Article  Google Scholar 

  2. 2

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

    Article  Google Scholar 

  3. 3

    Davies, N. B. & Welbergen, J. A. Social transmission of a host defense against cuckoo parasitism. Science 324, 1318–1320 (2009)

    ADS  CAS  Article  Google Scholar 

  4. 4

    Langmore, N. E., Cockburn, A., Russell, A. F. & Kilner, R. M. Flexible cuckoo chick-rejection rules in the superb fairy-wren. Behav. Ecol. 20, 978–984 (2009)

    Article  Google Scholar 

  5. 5

    Jenner, E. Observations on the natural history of the cuckoo. By Mr. Edward Jenner. In a letter to John Hunter, Esq. F. R. S. Phil. Trans. R. Soc. 78, 219–237 (1788)

    Article  Google Scholar 

  6. 6

    Dawkins, R. & Krebs, J. R. Arms races between and within species. Proc. R. Soc. B 205, 489–511 (1979)

    ADS  CAS  Google Scholar 

  7. 7

    Davies, N. B. Cuckoos, Cowbirds and Other Cheats (T. & A. D. Poyser, 2000)

    Google Scholar 

  8. 8

    Grim, T. The evolution of nestling discrimination by hosts of parasitic birds: why is rejection so rare? Evol. Ecol. Res. 8, 785–802 (2006)

    Google Scholar 

  9. 9

    Soler, M. Co-evolutionary arms race between brood parasites and their hosts at the nestling stage. J. Avian Biol. 40, 237–240 (2009)

    Article  Google Scholar 

  10. 10

    Lotem, A. Learning to recognize nestlings is maladaptive for cuckoo Cuculus canorus hosts. Nature 362, 743–745 (1993)

    ADS  Article  Google Scholar 

  11. 11

    Rothstein, S. I. Successes and failures in avian egg and nestling recognition with comments on the utility of optimality reasoning. Am. Zool. 22, 547–560 (1982)

    Article  Google Scholar 

  12. 12

    Davies, N. B. & Brooke, M. D. Cuckoos versus reed warblers—adaptations and counteradaptations. Anim. Behav. 36, 262–284 (1988)

    Article  Google Scholar 

  13. 13

    Langmore, N. E., Hunt, S. & Kilner, R. M. Escalation of a coevolutionary arms race through host rejection of brood parasitic young. Nature 422, 157–160 (2003)

    ADS  CAS  Article  Google Scholar 

  14. 14

    Britton, N. F., Planque, R. & Franks, N. R. Evolution of defence portfolios in exploiter–victim systems. Bull. Math. Biol. 69, 957–988 (2007)

    MathSciNet  CAS  Article  Google Scholar 

  15. 15

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

    Article  Google Scholar 

  16. 16

    Strausberger, B. M. & Rothstein, S. I. Parasitic cowbirds may defeat host defense by causing rejecters to misimprint on cowbird eggs. Behav. Ecol. 20, 691–699 (2009)

    Article  Google Scholar 

  17. 17

    Lawes, M. J. & Marthews, T. R. When will rejection of parasite nestlings by hosts of nonevicting avian brood parasites be favored? A misimprinting-equilibrium model. Behav. Ecol. 14, 757–770 (2003)

    Article  Google Scholar 

  18. 18

    Sato, N. J., Tokue, K., Noske, R. A., Mikami, O. K. & Ueda, K. Evicting cuckoo nestlings from the nest: a new anti-parasitism behaviour. Biol. Lett. 10.1098/rsbl.2009.0540 (23 September 2009)

  19. 19

    Lyon, B. E. & Eadie, J. M. A. Conspecific brood parasitism in birds: a life-history perspective. Annu. Rev. Ecol. Evol. Syst. 39, 343–363 (2008)

    Article  Google Scholar 

  20. 20

    Lyon, B. E. Conspecific brood parasitism as a flexible female reproductive tactic in American coots. Anim. Behav. 46, 911–928 (1993)

    Article  Google Scholar 

  21. 21

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

    ADS  CAS  Article  Google Scholar 

  22. 22

    Lyon, B. E., Hochachka, W. M. & Eadie, J. M. Paternity–parasitism trade-offs: a model and test of host–parasite cooperation in an avian conspecific brood parasite. Evolution 56, 1253–1266 (2002)

    Article  Google Scholar 

  23. 23

    Rothstein, S. I. Mechanisms of avian egg-recognition: additional evidence for learned components. Anim. Behav. 26, 671–677 (1978)

    Article  Google Scholar 

  24. 24

    Rodriguez-Girones, M. A. & Lotem, A. How to detect a cuckoo egg: a signal-detection theory model for recognition and learning. Am. Nat. 153, 633–648 (1999)

    PubMed  Google Scholar 

  25. 25

    Lyon, B. E., Eadie, J. M. & Hamilton, L. D. Parental choice selects for ornamental plumage in American coot chicks. Nature 371, 240–243 (1994)

    ADS  Article  Google Scholar 

  26. 26

    Rothstein, S. I. Experimental and teleonomic investigation of avian brood parasitism. Condor 77, 250–271 (1975)

    Article  Google Scholar 

  27. 27

    Horsfall, J. A. Brood reduction and brood division in coots. Anim. Behav. 32, 216–225 (1984)

    Article  Google Scholar 

  28. 28

    Briskie, J. V. & Sealy, S. G. Evolution of short incubation periods in the parasitic cowbirds, Molothrus spp. Auk 107, 789–794 (1990)

    Article  Google Scholar 

  29. 29

    Reed, W. L., Clark, M. E. & Vleck, C. M. Maternal effects increase within-family variation in offspring survival. Am. Nat. 174, 685–695 (2009)

    Article  Google Scholar 

  30. 30

    Foley, D. D. Use of colored markers on ducklings. N.Y. Fish Game J. 3, 240–247 (1956)

    Google Scholar 

  31. 31

    Lyon, B. E. Tactics of parasitic American coots—host choice and the pattern of egg dispersion among host nests. Behav. Ecol. Sociobiol. 33, 87–100 (1993)

    Article  Google Scholar 

  32. 32

    Gullion, G. W. Voice differences between sexes in the American coot. Condor 52, 272–273 (1950)

    Article  Google Scholar 

  33. 33

    R Development Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2009)

  34. 34

    Bates, D. & Maechler, M. lme4: Linear mixed-effects models using S4 classes. R package version 0. 999375-31 〈http://cran.r-project.org/web/packages/lme4/index.html〉 (2009)

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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.

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Correspondence to Daizaburo Shizuka.

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Supplementary information

Supplementary Information

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

41586_2010_BFnature08655_MOESM286_ESM.mov

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 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)

41586_2010_BFnature08655_MOESM287_ESM.mov

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 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)

41586_2010_BFnature08655_MOESM288_ESM.mov

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 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)

41586_2010_BFnature08655_MOESM289_ESM.mov

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 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)

41586_2010_BFnature08655_MOESM290_ESM.mov

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)

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. Nature 463, 223–226 (2010). https://doi.org/10.1038/nature08655

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