Emu Emu Society
Journal of BirdLife Australia
REVIEW

Helping behaviour and parental care in fairy-wrens (Malurus)

Nicolas Margraf A B and Andrew Cockburn A

A Evolution, Ecology and Genetics, Research School of Biology, The Australian National University, Canberra, ACT 0200, Australia.

B Corresponding author. Email: andrew.cockburn@anu.edu.au

Emu 113(3) 294-301 http://dx.doi.org/10.1071/MU13001
Submitted: 7 January 2013  Accepted: 13 June 2013   Published: 15 August 2013

Abstract

Cooperative breeding among birds was first discovered in the genus Malurus (Maluridae), the fairy-wrens. Cooperative care arises because male, and sometimes female, offspring remain in their natal territory and help the adults rear offspring. Early uses of data from Superb Fairy-wrens (Malurus cyaneus) to illustrate how kin altruism can explain helping behaviour were based on flawed assumptions. Most importantly, high rates of extra-group mating mean that the helpers often assist adults to which they are unrelated. However, measuring the costs and benefits of altruism has also proved difficult. Helping behaviour and its outcomes among species of Malurus are surprisingly diverse, despite similar founding conditions for cooperative breeding. First, species differ in whether help provides fitness benefits, in the recipients of those benefits, and whether benefits are immediate or deferred. Second, species vary greatly in whether females are philopatric and the extent to which female auxiliaries (supernumeraries), when present, provide care. Finally, male auxiliaries are much less sensitive to the needs of the brood than females. In this review we show that these three aspects of helping behaviour lack compelling explanations. We develop hypotheses to explain each phenomenon. Distinguishing among these hypotheses will greatly enhance our understanding of the remarkable social system of Malurus, and inform the study of cooperative breeding and sexual conflict in general.

Additional keywords: cooperative breeding, extra-pair copulation, helper at the nest, kin altruism, Maluridae, sexual conflict.


References

Boland, C. R. J., and Cockburn, A. (2002). Short sketches from the long history of cooperative breeding in Australian birds. Emu 102, 9–17.
Short sketches from the long history of cooperative breeding in Australian birds.CrossRef | open url image1

Bradley, E., and Bradley, J. (1958). Notes on the behaviours and plumage of colour-ringed blue wrens. Emu 58, 313–326.
Notes on the behaviours and plumage of colour-ringed blue wrens.CrossRef | open url image1

Brooker, M., and Rowley, I. (1995). The significance of territory size and quality in the mating strategy of the Splendid Fairy-wren. Journal of Animal Ecology 64, 614–627.
The significance of territory size and quality in the mating strategy of the Splendid Fairy-wren.CrossRef | open url image1

Brouwer, L., van de Pol, M., Atema, E., and Cockburn, A. (2011). Strategic promiscuity helps avoid inbreeding at multiple levels in a cooperative breeder where both sexes are philopatric. Molecular Ecology 20, 4796–4807.
Strategic promiscuity helps avoid inbreeding at multiple levels in a cooperative breeder where both sexes are philopatric.CrossRef | 22008256PubMed | open url image1

Brown, J. L. (1975). ‘The Evolution of Behavior.’ (WW Norton: New York.)

Brown, J. L. (1987). ‘Helping and Communal Breeding in Birds: Ecology and Evolution.’ (Princeton University Press: Princeton, NJ.)

Brown, J. L., Brown, E. R., Brown, S. D., and Dow, D. D. (1982). Helpers: effects of experimental removal on reproductive success. Science 215, 421–422.
Helpers: effects of experimental removal on reproductive success.CrossRef | 1:STN:280:DC%2BC3cvktFKhuw%3D%3D&md5=3fbd62d55de4ad2385b5627dac88c418CAS | 17814957PubMed | open url image1

Cockburn, A. (1998). Evolution of helping behavior in cooperatively breeding birds. Annual Review of Ecology and Systematics 29, 141–177.
Evolution of helping behavior in cooperatively breeding birds.CrossRef | open url image1

Cockburn, A. (2004). Mating systems and sexual conflict. In ‘Ecology and Evolution of Cooperative Breeding in Birds’. (Eds W. D. Koenig and J. L. Dickinson.) pp. 81–101. (Cambridge University Press: Cambridge, UK.)

Cockburn, A. (2006). Prevalence of different modes of parental care in birds. Proceedings of the Royal Society of London – B. Biological Sciences 273, 1375–1383.
Prevalence of different modes of parental care in birds.CrossRef | open url image1

Cockburn, A. (2013). Cooperative breeding in birds: towards a richer conceptual framework. In ‘Cooperation and its Evolution’. (Eds K. Sterelny, R. Joyce, B. Calcott and B. Fraser.) pp. 223–245. (MIT Press: Cambridge, MA.)

Cockburn, A., and Double, M. C. (2008). Cooperatively breeding Superb Fairy-wrens show no facultative manipulation of offspring sex ratio despite plausible benefits. Behavioral Ecology and Sociobiology 62, 681–688.
Cooperatively breeding Superb Fairy-wrens show no facultative manipulation of offspring sex ratio despite plausible benefits.CrossRef | open url image1

Cockburn, A., Osmond, H. L., Mulder, R. A., Green, D. J., and Double, M. C. (2003). Divorce, dispersal and incest avoidance in the cooperatively breeding Superb Fairy-wren Malurus cyaneus. Journal of Animal Ecology 72, 189–202.
Divorce, dispersal and incest avoidance in the cooperatively breeding Superb Fairy-wren Malurus cyaneus.CrossRef | open url image1

Cockburn, A., Osmond, H. L., and Double, M. C. (2008a). Swingin’ in the rain: condition dependence and sexual selection in a capricious world. Proceedings of the Royal Society of London – B. Biological Sciences 275, 605–612.
Swingin’ in the rain: condition dependence and sexual selection in a capricious world.CrossRef | open url image1

Cockburn, A., Osmond, H. L., Mulder, R. A., Double, M. C., and Green, D. J. (2008b). Demography of male reproductive queues in cooperatively breeding Superb Fairy-wrens Malurus cyaneus. Journal of Animal Ecology 77, 297–304.
Demography of male reproductive queues in cooperatively breeding Superb Fairy-wrens Malurus cyaneus.CrossRef | 18070042PubMed | open url image1

Cockburn, A., Sims, R. A., Osmond, H. L., Green, D. J., Double, M. C., and Mulder, R. A. (2008c). Can we measure the benefits of help in cooperatively breeding birds: the case of Superb Fairy-wrens Malurus cyaneus? Journal of Animal Ecology 77, 430–438.
Can we measure the benefits of help in cooperatively breeding birds: the case of Superb Fairy-wrens Malurus cyaneus?CrossRef | 18312341PubMed | open url image1

Cockburn, A., Dalziell, A. H., Blackmore, C. J., Double, M. C., Kokko, H., Osmond, H. L., Beck, N. R., Head, M. L., and Wells, K. (2009). Superb Fairy-wren males aggregate into hidden leks to solicit extragroup fertilizations before dawn. Behavioral Ecology 20, 501–510.
Superb Fairy-wren males aggregate into hidden leks to solicit extragroup fertilizations before dawn.CrossRef | open url image1

Cockburn, A., Brouwer, L., Double, M., Margraf, N., and van de Pol, M. (2013). Evolutionary origins and persistence of infidelity in Malurus: the least faithful birds. Emu 113, 208–217.
Evolutionary origins and persistence of infidelity in Malurus: the least faithful birds.CrossRef | open url image1

Colombelli-Négrel, D., and Kleindorfer, S. (2010). Video nest monitoring reveals male coloration-dependant nest predation and sex differences in prey size delivery in a bird under high sexual selection. Journal of Ornithology 151, 507–512.
Video nest monitoring reveals male coloration-dependant nest predation and sex differences in prey size delivery in a bird under high sexual selection.CrossRef | open url image1

Dalziell, A. H., and Cockburn, A. (2008). Dawn song in Superb Fairy-wrens: a bird that seeks extrapair copulations during the dawn chorus. Animal Behaviour 75, 489–500.
Dawn song in Superb Fairy-wrens: a bird that seeks extrapair copulations during the dawn chorus.CrossRef | open url image1

Davies, N. B., and Hatchwell, B. J. (1992). The value of male parental care and its influence on reproductive allocation by male and female Dunnocks. Journal of Animal Ecology 61, 259–272.
The value of male parental care and its influence on reproductive allocation by male and female Dunnocks.CrossRef | open url image1

Dickinson, J. L., and Hatchwell, B. J. (2004). Fitness consequences of helping. In ‘Ecology and Evolution of Cooperative Breeding in Birds’. (Eds W. D. Koenig and J. L. Dickinson.) pp. 48–66. (Cambridge University Press: Cambridge, UK.)

Double, M. C., and Cockburn, A. (2003). Subordinate Superb Fairy-wrens (Malurus cyaneus) parasitize the reproductive success of attractive dominant males. Proceedings of the Royal Society of London – B. Biological Sciences 270, 379–384.
Subordinate Superb Fairy-wrens (Malurus cyaneus) parasitize the reproductive success of attractive dominant males.CrossRef | open url image1

Dunn, P. O., and Cockburn, A. (1996). Evolution of male parental care in a bird with almost complete cuckoldry. Evolution 50, 2542–2548.
Evolution of male parental care in a bird with almost complete cuckoldry.CrossRef | open url image1

Dunn, P. O., and Cockburn, A. (1999). Extrapair mate choice and honest signaling in cooperatively breeding Superb Fairy-wrens. Evolution 53, 938–946.
Extrapair mate choice and honest signaling in cooperatively breeding Superb Fairy-wrens.CrossRef | open url image1

Dunn, P. O., Cockburn, A., and Mulder, R. A. (1995). Fairy-wren helpers often care for young to which they are unrelated. Proceedings of the Royal Society of London – B. Biological Sciences 259, 339–343.
Fairy-wren helpers often care for young to which they are unrelated.CrossRef | open url image1

Ekman, J., Hatchwell, B. J., Dickinson, J. L., and Griesser, M. (2004). Delayed dispersal. In ‘Ecology and Evolution of Cooperative Breeding in Birds’. (Eds W. D. Koenig and J. L. Dickinson.) pp. 35–47. (Cambridge University Press: Cambridge, UK.)

Emlen, S. T. (1982). The evolution of helping. I. An ecological constraints model. American Naturalist 119, 29–39.
The evolution of helping. I. An ecological constraints model.CrossRef | open url image1

Emlen, S. T. (1997). Predicting family dynamics in social vertebrates. In ‘Behavioural Ecology: An Evolutionary Approach’. 4th edn. (Eds J. R. Krebs and N. B. Davies.) pp. 228–53. (Blackwell Science: Oxford, UK.)

Grafen, A. (1984). Natural selection, kin selection and group selection. In ‘Behavioural Ecology: An Evolutionary Approach’. 2nd edn. (Eds J. R. Krebs and N. B. Davies.) pp. 62–84. (Blackwell Scientific Publications: Oxford, UK.)

Green, D. J., Cockburn, A., Hall, M. L., Osmond, H., and Dunn, P. O. (1995). Increased opportunities for cuckoldry may be why dominant male fairy-wrens tolerate helpers. Proceedings of the Royal Society of London – B. Biological Sciences 262, 297–303.
Increased opportunities for cuckoldry may be why dominant male fairy-wrens tolerate helpers.CrossRef | open url image1

Green, D. J., Osmond, H. L., Double, M. C., and Cockburn, A. (2000). Display rate by male fairy-wrens (Malurus cyaneus) during the fertile period of females has little influence on extra-pair mate choice. Behavioral Ecology and Sociobiology 48, 438–446.
Display rate by male fairy-wrens (Malurus cyaneus) during the fertile period of females has little influence on extra-pair mate choice.CrossRef | open url image1

Higgins, P. J., Peter, J. M., and Steele, W. K. (Eds) (2001). ‘Handbook of Australian, New Zealand and Antarctic Birds. Vol. 5: Tyrant-flycatchers to Chats.’ (Oxford University Press: Melbourne.)

Kingma, S. A., Hall, M. L., Segelbacher, G., and Peters, A. (2009). Radical loss of an extreme extra-pair mating system. BMC Ecology 9, 15.
Radical loss of an extreme extra-pair mating system.CrossRef | 19454026PubMed | open url image1

Kingma, S. A., Hall, M. L., Arriero, E., and Peters, A. (2010). Multiple benefits of cooperative breeding in Purple-crowned Fairy-wrens: a consequence of fidelity? Journal of Animal Ecology 79, 757–768.
| 20443991PubMed | open url image1

Kingma, S. A., Hall, M. L., and Peters, A. (2011). Multiple benefits drive helping behavior in a cooperatively breeding bird: an integrated analysis. American Naturalist 177, 486–495.
Multiple benefits drive helping behavior in a cooperatively breeding bird: an integrated analysis.CrossRef | 21460570PubMed | open url image1

Kokko, H., Johnstone, R. A., and Clutton-Brock, T. H. (2001). The evolution of cooperative breeding through group augmentation. Proceedings of the Royal Society of London – B. Biological Sciences 268, 187–196.
The evolution of cooperative breeding through group augmentation.CrossRef | 1:STN:280:DC%2BD3MzmsleqtQ%3D%3D&md5=0878f6e26b3fcc0b1464d340c540753fCAS | open url image1

Komdeur, J. (1992). Importance of habitat saturation and territory quality for evolution of cooperative breeding in the Seychelles Warbler. Nature 358, 493–495.
Importance of habitat saturation and territory quality for evolution of cooperative breeding in the Seychelles Warbler.CrossRef | open url image1

Langmore, N. E., Hunt, S., and Kilner, R. M. (2003). Escalation of a coevolutionary arms race through host rejection of brood parasitic young. Nature 422, 157–160.
Escalation of a coevolutionary arms race through host rejection of brood parasitic young.CrossRef | 1:CAS:528:DC%2BD3sXhvFKgsrk%3D&md5=366c29e6dada99a2dd2bb5d34d68df49CAS | 12634784PubMed | open url image1

MacGregor, N. A., and Cockburn, A. (2002). Sex differences in parental response to begging nestlings in Superb Fairy-wrens. Animal Behaviour 63, 923–932.
Sex differences in parental response to begging nestlings in Superb Fairy-wrens.CrossRef | open url image1

Magrath, R. D., and Yezerinac, S. M. (1997). Facultative helping does not influence reproductive success or survival in cooperatively breeding White-browed Scrubwrens. Journal of Animal Ecology 66, 658–670.
Facultative helping does not influence reproductive success or survival in cooperatively breeding White-browed Scrubwrens.CrossRef | open url image1

Maguire, G. S., and Mulder, R. A. (2004). Breeding biology and demography of the Southern Emu-wren (Stipiturus malachurus). Australian Journal of Zoology 52, 583–604.
Breeding biology and demography of the Southern Emu-wren (Stipiturus malachurus).CrossRef | open url image1

Mulder, R. A. (1997). Extra-group courtship displays and other reproductive tactics of Superb Fairy-wrens. Australian Journal of Zoology 45, 131–143.
Extra-group courtship displays and other reproductive tactics of Superb Fairy-wrens.CrossRef | open url image1

Mulder, R. A., and Langmore, N. E. (1993). Dominant males punish helpers for temporary defection in Superb Fairy-wrens. Animal Behaviour 45, 830–833.
Dominant males punish helpers for temporary defection in Superb Fairy-wrens.CrossRef | open url image1

Mulder, R. A., Dunn, P. O., Cockburn, A., Lazenby-Cohen, K. A., and Howell, M. J. (1994). Helpers liberate female fairy-wrens from constraints on extra-pair mate choice. Proceedings of the Royal Society of London – B. Biological Sciences 255, 223–229.
Helpers liberate female fairy-wrens from constraints on extra-pair mate choice.CrossRef | open url image1

Mumme, R. L., Koenig, W. D., and Ratnieks, F. L. W. (1989). Helping behaviour, reproductive value, and the future component of indirect fitness. Animal Behaviour 50, 607–621. open url image1

Murphy, S. A., Legge, S. M., Heathcote, J., and Mulder, E. (2010). The effects of early and late-season fires on mortality, dispersal, physiology and breeding of Red-backed Fairy-wrens (Malurus melanocephalus). Wildlife Research 37, 145–155.
The effects of early and late-season fires on mortality, dispersal, physiology and breeding of Red-backed Fairy-wrens (Malurus melanocephalus).CrossRef | open url image1

Nakagawa, S., Gillespie, D. O. S., Hatchwell, B. J., and Burke, T. (2007). Predictable males and unpredictable females: sex difference in repeatability of parental care in a wild bird population. Journal of Evolutionary Biology 20, 1674–1681.
Predictable males and unpredictable females: sex difference in repeatability of parental care in a wild bird population.CrossRef | 1:STN:280:DC%2BD2svpsFGgug%3D%3D&md5=2c3d19749107ea9b34f57ab5ca6a5464CAS | 17714284PubMed | open url image1

Peters, A. (2002). Testosterone and the trade-off between mating and paternal effort in extrapair-mating Superb Fairy-wrens. Animal Behaviour 64, 103–112.
Testosterone and the trade-off between mating and paternal effort in extrapair-mating Superb Fairy-wrens.CrossRef | open url image1

Peters, A., Astheimer, L. B., Boland, C. R. J., and Cockburn, A. (2000). Testosterone is involved in acquisition and maintenance of sexually selected male plumage in Superb Fairy-wrens, Malurus cyaneus. Behavioral Ecology and Sociobiology 47, 438–445.
Testosterone is involved in acquisition and maintenance of sexually selected male plumage in Superb Fairy-wrens, Malurus cyaneus.CrossRef | open url image1

Peters, A., Astheimer, L. B., and Cockburn, A. (2001). The annual testosterone profile in cooperatively breeding Superb Fairy-wrens, Malurus cyaneus, reflects their extreme infidelity. Behavioral Ecology and Sociobiology 50, 519–527.
The annual testosterone profile in cooperatively breeding Superb Fairy-wrens, Malurus cyaneus, reflects their extreme infidelity.CrossRef | open url image1

Peters, A., Cockburn, A., and Cunningham, R. (2002). Testosterone treatment suppresses paternal care in Superb Fairy-wrens, Malurus cyaneus, despite their concurrent investment in courtship. Behavioral Ecology and Sociobiology 51, 538–547.
Testosterone treatment suppresses paternal care in Superb Fairy-wrens, Malurus cyaneus, despite their concurrent investment in courtship.CrossRef | open url image1

Pruett-Jones, S. G., and Lewis, M. J. (1990). Sex ratio and habitat limitation promote delayed dispersal in Superb Fairy-wrens. Nature 348, 541–542.
Sex ratio and habitat limitation promote delayed dispersal in Superb Fairy-wrens.CrossRef | open url image1

Remeš, V., Matysiokova, B., and Cockburn, A. (2012). Long-term and large-scale analyses of nest predation patterns in Australian songbirds and a global comparison of nest predation rates. Journal of Avian Biology 43, 435–444.
Long-term and large-scale analyses of nest predation patterns in Australian songbirds and a global comparison of nest predation rates.CrossRef | open url image1

Rowley, I. (1957). Cooperative feeding of young by Superb Blue Wrens. Emu 57, 356–357.
Cooperative feeding of young by Superb Blue Wrens.CrossRef | open url image1

Rowley, I. (1964). The life history of the Superb Blue Wren. Emu 64, 251–297.
The life history of the Superb Blue Wren.CrossRef | open url image1

Rowley, I., and Russell, E. (1997). ‘Fairy-wrens and Grasswrens: Maluridae.’ (Oxford University Press: Oxford, UK.)

Royle, N. J., Schuett, W., and Dall, S. R. X. (2010). Behavioral consistency and the resolution of sexual conflict over parental investment. Behavioral Ecology 21, 1125–1130.
Behavioral consistency and the resolution of sexual conflict over parental investment.CrossRef | open url image1

Russell, E., and Rowley, I. (1988). Helper contributions to reproductive success in the Splendid Fairy-wren (Malurus splendens). Behavioral Ecology and Sociobiology 22, 131–140.
Helper contributions to reproductive success in the Splendid Fairy-wren (Malurus splendens).CrossRef | open url image1

Russell, E. M., and Rowley, I. (1993a). Demography of the cooperatively breeding Splendid Fairy-wren, Malurus splendens (Maluridae). Australian Journal of Zoology 41, 475–505.
Demography of the cooperatively breeding Splendid Fairy-wren, Malurus splendens (Maluridae).CrossRef | open url image1

Russell, E. M., and Rowley, I. (1993b). Philopatry or dispersal: competition for territory vacancies in the Splendid Fairy-wren, Malurus splendens. Animal Behaviour 45, 519–539.
Philopatry or dispersal: competition for territory vacancies in the Splendid Fairy-wren, Malurus splendens.CrossRef | open url image1

Russell, E., and Rowley, I. (2000). Demography and social organisation of the Red-winged Fairy-wren, Malurus elegans. Australian Journal of Zoology 48, 161–200.
Demography and social organisation of the Red-winged Fairy-wren, Malurus elegans.CrossRef | open url image1

Russell, A. F., Langmore, N. E., Cockburn, A., Astheimer, L. B., and Kilner, R. M. (2007). Reduced egg investment can conceal helper effects in cooperatively breeding birds. Science 317, 941–944.
Reduced egg investment can conceal helper effects in cooperatively breeding birds.CrossRef | 1:CAS:528:DC%2BD2sXptVaju7s%3D&md5=2ffaeb826ed6cd49d58eb9f938945131CAS | 17702942PubMed | open url image1

Russell, A. F., Langmore, N. E., Gardner, J. L., and Kilner, R. M. (2008). Maternal investment tactics in Superb Fairy-wrens. Proceedings of the Royal Society of London – B. Biological Sciences 275, 29–36.
Maternal investment tactics in Superb Fairy-wrens.CrossRef | 1:STN:280:DC%2BD2snptFKisQ%3D%3D&md5=2dc4bde16d5c972fd62ae983d703202bCAS | open url image1

Schodde, R., and Weatherly, R. (1982). ‘The Fairy-wrens: a Monograph of the Maluridae.’ (Lansdowne: Melbourne.)

Schuett, W., Tregenza, T., and Dall, S. R. X. (2010). Sexual selection and animal personality. Biological Reviews of the Cambridge Philosophical Society 85, 217–246.
Sexual selection and animal personality.CrossRef | 19922534PubMed | open url image1

Tidemann, S. C. (1986). Breeding in three species of fairy-wrens (Malurus): do helpers really help? Emu 86, 131–138.
Breeding in three species of fairy-wrens (Malurus): do helpers really help?CrossRef | open url image1

Van Bael, S., and Pruett-Jones, S. (2000). Breeding biology and social behaviour of the eastern race of the Splendid Fairy-wren Malurus splendens melanotus. Emu 100, 95–108.
Breeding biology and social behaviour of the eastern race of the Splendid Fairy-wren Malurus splendens melanotus.CrossRef | open url image1



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