• communal breeding;
  • delayed dispersal;
  • helpers-at-the-nest;
  • kin-selection;
  • mixed model;
  • parental investment;
  • philopatry;
  • promiscuity


  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Supporting Information

1. Kin selection is one of the mechanisms that can explain apparent altruism by subordinate individuals in cooperatively breeding species, if subordinates boost the production of kin. We compared productivity and breeder survival in pairs with and without subordinates in a genetically monogamous cooperatively breeding bird, the purple-crowned fairy-wren Malurus coronatus.

2. Additive effects of subordinate help increased productivity. Total feeding rates to the nest were increased by two or more subordinates, and fledgling production was greater in larger groups. Not all subordinates contributed to nestling feeding, and the effect of group size was greater when non-contributors were excluded from analyses, suggesting that increased fledgling production was a direct result of help.

3. Compensatory effects of subordinate help improved breeder survival. Assisted breeders reduced their workload by 20–30%, irrespective of the number of helpers. Although re-nesting intervals were not affected by group size, reduced breeder feeding rates resulted in improved survival and breeders in larger groups survived better.

4. Subordinates and nestlings are usually progeny of the breeding pair in this species, and benefits of cooperative breeding are very different from three congeners with extremely high levels of extra-group paternity (EGP). In these Malurus, fledgling production and survival of male breeders are not enhanced in larger groups. This is consistent with the expectation that kin-selected benefits vary with relatedness, and thus levels of EGP.

5. We tested whether benefits of cooperative breeding in 37 avian species varied with levels of extra-group mating. Both direct and phylogenetically controlled comparisons showed that improvement of (male) breeder survival and enhanced productivity are more likely when fidelity is higher, as predicted when investment of subordinates correlates with relatedness to offspring. This pattern highlights the importance of considering the genetic mating system for understanding the evolution of cooperative breeding.


  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Supporting Information

In cooperatively breeding species, subordinate individuals forego their own reproduction to assist the breeding pair in the rearing of usually non-descendant offspring (Brown 1987; Stacey & Koenig 1990; Cockburn 1998). The adaptive basis of cooperative breeding and such seemingly altruistic behaviour has been discussed extensively, but remains a highly debated topic to date (Cockburn 1998; Dickinson & Hatchwell 2004; Lehmann & Keller 2006; Hatchwell 2009). However, it has generally been recognized that for cooperative breeding to be evolutionarily stable, there must be benefits for both the subordinate individuals and the breeders that accommodate them. Determining such benefits is therefore crucial for our understanding of the evolution and maintenance of cooperative breeding.

Several direct and indirect benefits of cooperative breeding have been proposed (see, e.g. Emlen & Wrege 1989; Cockburn 1998; Dickinson & Hatchwell 2004). Breeders can benefit if subordinates enhance their reproductive output (Cockburn 1998; Hatchwell 1999) or survival (Crick 1992; Khan & Walters 2002). Subordinates can obtain direct benefits, like parentage (e.g. Hartley & Davies 1994; Li & Brown 2002; Richardson, Burke & Komdeur 2002), or benefits of group living (e.g. Gaston 1978; Kokko, Johnstone & Wright 2002). In addition, future benefits may be important, for instance when subordinates can inherit the territory (e.g. Ligon & Ligon 1978), and therefore subordinates may benefit from raising offspring that later become helpers (group augmentation; e.g. Kokko, Johnstone & Clutton-Brock 2001). Third, inclusive fitness benefits may apply when subordinates increase productivity of close relatives (indirect kin-selected benefits; Hamilton 1964).

Many benefits of cooperative breeding depend on enhanced reproductive output. This can result directly from an improvement in the outcome of the current reproductive attempt (see Cockburn 1998; Hatchwell 1999). Alternatively or additionally, subordinates can positively influence future reproduction through increased breeder survival (see Khan & Walters 2002) or shortened intervals between reproductive attempts (e.g. Brown & Brown 1981; Innes & Johnston 1996; Langen & Vehrencamp 1999; Woxvold & Magrath 2005; Canestrari, Marcos & Baglione 2008). Which effects prevail (future or current benefits) may depend on whether assisted breeders decrease investment (compensatory effects; Crick 1992; Khan & Walters 2002) or maintain similar effort, so that subordinate assistance is additive (Cockburn 1998; Hatchwell 1999; Legge 2000b; Heinsohn 2004).

Subordinates can benefit from helping if they derive inclusive fitness from enhanced production of related individuals (Emlen 1995, 1997; Emlen & Wrege 1989; Griffin & West 2003; Hamilton 1964; for other benefits see Cockburn 1998). As provisioning of care to dependent young is costly (Bryant 1988; Heinsohn & Legge 1999), subordinates are expected to adjust their contribution according to potential benefits and, assuming that kin selection plays an important role, invest more in closely related offspring (Hamilton 1964; Komdeur 1994; Griffin & West 2003). Thus, the genetic mating system may modulate effects of group size: in species with high levels of mating outside the group, offspring are less related to subordinates, and consequently indirect benefits are lower. If subordinates adjust care accordingly, the effects of subordinates on productivity may depend on the level of extra-group paternity (EGP). Surprisingly however, such a role of extra-group mating in shaping benefits of cooperative breeding has, as far as we are aware, not been explicitly considered among cooperatively breeding vertebrates (see Hatchwell 1999; Cockburn 2004).

Here, we investigate whether group size is related to current (offspring production) or future (breeder survival and re-nesting interval) productivity in purple-crowned fairy-wrens Malurus coronatus. In addition, we explore nestling feeding rates as a mechanism behind observed effects. M. coronatus is genetically nearly monogamous (Kingma et al. 2009), and a remarkable exception in the genus Malurus, which has some of the highest known levels of extra-pair paternity reported in birds (Brooker et al. 1990; Mulder et al. 1994; Griffith, Owens & Thuman 2002; Karubian 2002; Webster et al. 2004; Webster, Varian & Karubian 2008; Kingma et al. 2009). Therefore, we explicitly compare benefits of cooperative breeding between Malurus species. Finally, we conduct a phylogenetically controlled comparative analysis of the effects of subordinates in all cooperatively breeding birds with known levels of EGP, to establish whether the genetic mating system might play a role in the nature of benefits of cooperative breeding in general.

Materials and methods

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Supporting Information

Study site and species

A population of between 33 and 48 M. coronatus groups was studied from March 2006 to September 2008 at Mornington Wildlife Sanctuary, in north-west Australia (S17°31′ E126°6′). The study site consists of about 8 km of riparian vegetation along Annie Creek and the Adcock River. M. coronatus are riparian specialists endemic to the northern tropics of Australia, and are restricted to creeks and rivers, rarely venturing more than 20 m from the riverbed (Rowley & Russell 1997, personal observations). Territories are arranged linearly along rivers occupying both riverbanks, and are maintained throughout the year (Hall & Peters 2008, 2009). M. coronatus breed cooperatively, and live in socially monogamous pairs (breeders) with between 40% and 70% of pairs being accompanied by on average between 1 and 2 male and/or female subordinates (range 0–9 subordinates; Rowley & Russell 1997, personal observations). Nesting occurs primarily in the wet season, but birds can breed opportunistically in any month (Rowley & Russell 1993, 1997, personal observations). Nests are built and eggs incubated exclusively by the breeder female. Clutch size is 1–4 eggs (median 3); incubation lasts around 14 days and the nestling period lasts for about 13 days (personal observations). Subordinates assist the dominant pair in feeding the nestlings (Rowley & Russell 1993).

Population and nest monitoring

All individuals in our study population were banded with a unique combination of three plastic colour bands and a numbered metal band. Sex was determined on the basis of sex-specific plumage characteristics (see Rowley & Russell 1997). Weekly population censuses documented group size, survival and social status of each group member, and nesting activity. A group member was defined as an individual within a given territory present for a minimum of 2 weeks. Each bird in a group could be unambiguously assigned dominant or subordinate status from behavioural cues (the most distinctive being that only the dominant pair participates in a song duet; Hall & Peters 2008, 2009).

Females were observed weekly for signs of nesting activity. Once found, nests were checked regularly to determine clutch size, hatching date and number of nestlings. Nestlings were banded when they were c. 7 days old (average banding age ± SE = 7·4 ± 0·13 days, range = 5–12, = 111 broods). Number of fledglings was determined by inspecting the territory around the day when fledging was expected. The average (±SE) number of days between expected fledging date and determination of number of fledglings was 1·8 ± 0·22 days (= 76, range = 0–9 days) and this interval did not predict the proportion of nestlings at banding that fledged, indicating that potential bias of early fledgling mortality is negligible (generalized linear model with number of nestlings as binomial total, number of fledglings as response variable and number of days after expected fledge date as explanatory variable: = 68 broods, Wald = 0·40, P = 0·53).

Group size

Breeders were defined as the dominant breeding male and female, and ‘group size’ includes the breeding pair and all subordinates. Juveniles (subordinates less than 145 days old, the youngest age a subordinate bird was observed feeding nestlings) were not included in our measure of ‘group size’. Some subordinate individuals did not contribute to nestling feeding (18 of 80 subordinates in 13 out of 39 nests with subordinates). Therefore, the analyses were repeated with ‘number of helpers’, defined as individuals that contributed to nestling feeding in at least one nest watch (see next). Group size (2, 3 and 4+) and ‘number of helpers’ (0, 1 and 2+) were grouped into three categories as cases with more than two subordinates or helpers were rare (11 and 7 of 73 observed nests, respectively).

Nest observations

Between September 2006 and September 2008, we conducted 266 nest watches at 73 nests on 39 territories, recording the total feeding rate (number of visits to the nest per hour) and the individual feeding rate for each group member. Group members could generally be unambiguously identified by their colour rings, except for 67 feeding visits (<2% of 3610 feeding visits recorded in total) in 38 nest watches of 25 nests in 19 territories. Generally, four nest watches (mean ± SE: 3·63 ± 0·10; range: 1–5) were conducted on usually consecutive days between 4 and 10 days after hatching, alternating morning (a.m.; 5:30–11:00) and afternoon (p.m.; 14:00–18:00), with the timing of the first nest watch randomly determined. The duration of nest watches was generally 60 min (mean ± SE = 60·1 ± 0·26; range: 30–90 min).

Statistical analyses

For analyses, a mixed modelling approach in Genstat 11·0 was used. By fitting random factors in the model, mixed models allow correcting for hierarchical repeated sampling (Schall 1991). For continuous response variables, restricted maximum likelihood models (REML) were used. For binary and count (poisson) data, generalized linear mixed models (GLMMs) were used with logit link (with binomial totals of 1) and log-link functions, respectively. All explanatory variables and relevant interactions were included initially, and the variable with the highest P-value was removed stepwise, leading to a final model with only significant terms (P < 0·05). Reported values of non-significant variables were obtained after re-inclusion in the final (significant) model. We present effect sizes, (back-transformed) means, and significance details as predicted by the full models in the text and tables, but in the figures we present raw data. To meet model assumptions, residuals of final REML models were checked for normality, and response variables were transformed when residuals were not normally distributed (see next). Random factors with a negative component of variance were omitted from the models. Where relevant, post hoc tests were conducted by testing whether differences between categories were larger than the calculated least significant differences (LSD) at 5%, 1% and 0·1% levels. As post hoc tests were not available for GLMMs, categorical differences were assessed by restricting original analyses to the subset of data of relevant categories.

Recently, it has been argued that penalized quasi-likelihood parameter estimation, as implemented in Genstat, could be problematic for GLMMs with binomial or poisson data (Bolker et al. 2009). This was not the case for our analyses as repeating the statistical models using Laplace approximation for parameter estimation in the lme4 package (Bates & Sarkar 2007) in R 2·8·2 (R development Core Team 2009) yielded very similar results (data not shown).

Analyses of productivity

We tested whether ‘group size’ affected the following variables: clutch size, number of fledglings, breeder survival and re-nesting interval. As group size effects caused by helping may be better predicted by number of helpers or feeding rates (e.g. Davies & Hatchwell 1992), we repeated these analyses, replacing ‘group size’ with ‘number of helpers’ and then with ‘feeding rate’ (mean total feeding rate or mean individual feeding rate averaged per nest) where possible (see next).

The effect of ‘group size’ and ‘number of helpers’ on clutch size and number of fledglings (poisson distribution) was tested using GLMMs with ‘breeding pair identity (ID)’ as a random factor. Only nests that were at least partly successful (i.e. produced fledglings) and two nests that contained dead nestlings were included in the analyses of fledgling success; nests that failed completely owing to flooding, nest collapse, disappearance of the entire brood, interspecific brood parasitism or disappearance of one of the parents, were not included.

Survival of breeders was expressed as likelihood of surviving until the next reproductive attempt. We obtained information on breeder survival from weekly territory censuses. We did not use a mark–recapture approach as ‘recapture rates’ were high: we resighted more than 95% of birds each week throughout the year (unpublished data). Moreover, including all nests in the study period, breeders survived in 440 of 474 (93%) cases until the next reproductive attempt. Our estimates of survival were unlikely to be confounded by dispersal of breeders outside the study site as we confirmed that this was rare with annual surveys of over 90% of suitable habitat within a 20 km radius of the study site (unpublished data).

To avoid pseudoreplication of individuals with multiple nests, only the last nest of individuals that did not survive and the penultimate nest for those that did survive until a next nesting attempt were used. GLMM analyses with the random term ‘territory-ID’ were used for analyses with ‘group size’ as explanatory variable. Males and females were analysed together by adding ‘sex’ as a factor, but survival was not different between males and females (Wald = 0·04, P = 0·84) and effects of group size on survival did not depend on breeder sex (interaction effect: Wald = 0·02, P = 0·99). Brood size (Wald = 0·06, P = 0·97) and the number of days individuals cared for nestlings/fledglings (with a maximum of 105 days when fledglings are independent; Wald = 1·36, P = 0·25) did not affect survival. For the analyses of the effect of number of helpers on breeder survival the last (or penultimate; see before) nest for which feeding watches were conducted were used. Sample sizes when including ‘number of helpers’ and ‘feeding rates’ as explanatory variable were reduced to the subset of nests at which feeding watches were conducted. To avoid overparameterized models, we included only ‘breeder sex’ as an additional explanatory variable in these GLMMs, but also in this model survival was not different between males and females (Wald = 0·92, P = 0·35).

Re-nesting interval was expressed as the logarithm of number days between end of a nest (failure date or fledging date) and initiation (first egg) of the next nest per pair. Re-nesting interval was analysed using REML models with ‘female-ID’ as a random term. ‘Female-ID’ revealed negative variance in the model with ‘number of helpers’ and the model with ‘feeding rate’ as the dependent variable, and was omitted from these models. Brood size did not affect re-nesting interval (in all models Wald < 3·37 and P > 0·19), but the significant positive effect of the number of days the offspring survived (in all models Wald > 14·75 and P < 0·001) was corrected for.

Analyses of feeding rates

To investigate whether ‘group size’ and ‘number of helpers’ influence total feeding rate and individual feeding rates of dominant breeders (response terms, square-root-transformed to normalize model residuals), REML models were used with control for random factors (‘territory-ID’ and ‘nest-ID within territory-ID’ in analyses of total feeding rate and ‘bird-ID’ and ‘nest-ID within bird-ID’ in analyses of breeder feeding rates; territory-ID showed negative variance in analyses of breeder feeding rates and was not included). Brood size and wind intensity were corrected for in the model, as larger broods were fed more often overall and by individuals (in all models Wald > 39·41 and P < 0·001), and feeding rates were lower when conditions were very windy, compared with no or light wind (in all models Wald > 8·90 and P < 0·014). In addition, females were observed brooding younger nestlings mainly in the morning and, as brooding may affect feeding rates, we corrected for the significant interaction between whether a nest watch was done in the morning or afternoon and age of the brood (in all models Wald > 9·83 and P < 0·003). In the analyses of breeder feeding rate, sex of the focal birds was added, but feeding rates were not different between males and females (in both models Wald < 0·92 and P > 0·34), and neither did effects of group size or number of helpers on breeder feeding rate depend on sex of the breeder (interaction effects; in both models Wald < 0·80 and P > 0·67). Nest watches where one or more visiting birds could not be identified were omitted from these analyses.

Comparative study

A systematic search was conducted for literature providing levels of EGP in altricial cooperatively breeding bird species, using review papers (Owens & Hartley 1998; Arnold & Owens 2002; Griffith, Owens & Thuman 2002), and the Web of Science (keywords: ‘parentage’ or ‘paternity’ and ‘cooperative’ or ‘birds’). Subsequently, for the species for which rates of EGP (for more than eight broods) are published, we investigated whether or not subordinates increased reproductive success and breeder survival, obtained from review papers (Cockburn 1998; Hatchwell 1999; Legge 2000b; Khan & Walters 2002), Web of Science (search on common and scientific species name) or directly from researchers. This resulted in a data set of 37 species, widely distributed throughout the Aves (28 genera, 22 families; see Table 2 and online Supporting Information). Although positive effects of subordinates may only become apparent after fledging in some species (e.g. Hatchwell et al. 2004), number of fledglings per nest was used as measure of reproductive success because these data are most widely available and therefore most suitable for standardized comparison between species. In addition, if effects of subordinates varied within species (e.g. with breeder female age, Magrath 2001, or brood size, Meade et al. 2010), the overall effect was used (see footnotes in Table 2).

Table 2.   The effect of subordinates in 37 cooperatively breeding bird species for which levels of extra-group paternity (EGP) are published. Listed are the levels of EGP, whether subordinates increase the number of fledglings per nest (reproductive success, RS), and whether subordinates increase survival probability of male and female breeders. Species were divided in two categories, where species with below- and above-median levels of EGP were, respectively, classified as ‘low EGP’ and ‘high EGP’
SpeciesEGPaIncreased RSbIncreased breeder survivalReferences
MaleFemaleEGPRS and survival
  1. aEGP, as the percentage of nests that contain at least one offspring sired by a male outside the cooperatively breeding group. We used extra-group instead of extra-pair paternity (EPP) to avoid complications of shared reproduction within groups in species with more complex mating systems (see, e.g. Cockburn 1998). bIncrease in number of fledglings per nest. cIt is unclear how many nests contain offspring sired by subordinate males and hence level of EPP is given. dOnly EPP is given, and this value is probably an overestimation of the rate of EGP. However, as within-group EPP is <2% (Webster, Varian & Karubian 2008), this overestimation is marginal. eEGP was not given for one population but EPP was also very high (Webster et al. 2004). fThe average of three studies in the same population. gEGP was also high but slightly lower in another subspecies Gymorhina titibcen tyrannical (Durrant & Hughes 2005). hThere was a positive correlation between group size and number of fledglings. The authors state, based on a pairwise comparison of reproductive success of groups that change in composition, that there is no positive effect. However, as Dickinson & Hatchwell (2004) outline, pairwise comparison likely underestimates true effects, and therefore we used the results of the correlative approach. iThere was a positive effect of group size in another population for which rates of EGP were unknown (Nakamura 1998). jSubordinates have a positive effect on reproductive success of yearling females (Magrath 2001). kNo distinction was made between adult subordinates and breeders, as both were included in analyses of the effects of group size on survival. lClear pattern but not quite significant at the 5% level. mSubordinates increase breeder male survival when broods are large (Meade et al. 2010). nNegative effect of subordinates.

  2. References: 1. Lundy, Parker & Zahavi (1998); 2. Quinn et al. (1999); 3. Woxvold & Mulder (2008); 4. Legge & Cockburn (2000); 5. Bruce et al. (1996); 6. Covas et al. (2006); 7. Heinsohn et al. (2000); 8. Faaborg et al. (1995); 9. Haydock, Koenig & Stanback (2001); 10. Mumme et al. (1985); 11. Hartley et al. (1995); 12. Brooke & Hartley (1995); 13. Haydock, Parker & Rabenold (1996); 14. Burke et al. (1989); 15. Haig, Belthoff & Allen (1993); 16. Haig, Walters & Plissner (1994); 17. Rabenold et al. (1990); 18. Wrege & Emlen (1987); 19. Kingma et al. (2009); 20. Jones, Lessells & Krebs (1991); 21. Baglione et al. (2002); 22. Poldmaa, Montgomerie & Boag (1995); 23. Conrad et al. 1998); 24. Rubenstein (2007a); 25. Temple, Hoffman & Amos (2009); 26. Hatchwell et al. (2002); 27. Seddon et al. (2005); 28. Blackmore & Heinsohn (2008); 29. Williams (2004); 30.Townsend et al. 2009); 31. Du & Lu (2009); 32.Whittingham, Dunn & Magrath (1997); 33. Berg (2005); 34. Richardson et al. (2001); 35. Dickinson & Akre (1998); 36. Webster, Varian & Karubian (2008); 37. Brooker et al. (1990); 38. Mulder & Magrath (1994); 39. Double & Cockburn (2000); 40. Green et al. (2000); 41. Hughes et al. 2003). 42. Wright (1998); 43. Zahavi (1974); 44. Ridley (2007); 45. Brown (1975); 46. Zahavi (1990); 47. Franzreb (2007); 48. Mumme (1992); 49. Stallcup & Woolfenden (1978); 50. Woolfenden & Fitzpatrick (1990); 51. Woolfenden (1981); 52. Woxvold & Magrath (2005); 53. Parry (1973); 54. Legge (2000a); 55. Sloane (1996); 56. R. Covas, unpublished data; 57. Covas, du Plessis & Doutrelant (2008); 58. R. Heinsohn, unpublished data; 59. Heinsohn (1995); 60. Beck & Heinsohn (2006); 61. Heinsohn (1992); 62. Boland, Heinsohn & Cockburn (1997); 63. Faaborg et al. (1980); 64. Faaborg (1986); 65. Faaborg & Bednarz (1990); 66. Koenig (1981); 67. Stacey (1979); 68. Koenig & Mumme (1987); 69. Koenig & Stacey (1990); 70. Davies et al. (1995); 71. Austad & Rabenold (1985); 72. Austad & Rabenold (1986); 73. Rabenold (1990); 74. Davies & Houston (1986); 75. Davies (1986); 76. Davies & Hatchwell (1992); 77. Davies (1990); 78. Davies (1992); 79. Houston & Davies (1985); 80. Khan & Walters (2002), 81. Lennartz, Hooper & Harlow (1987); 82. Lennartz & Harlow (1979); 83. Neal et al. (1993); 84. Heppell, Walters & Crowder (1994); 85. Rabenold (1984); 86. Emlen & Wrege (1991); 87. Emlen & Wrege (1989); 88. Emlen (1990); 89. Emlen (1981); 90. Emlen (1990); 91. This study; 92. Lessells (1990); 93. Canestrari, Marcos & Baglione (2008); 94. Dow & Whitmore (1990); 95. Poiani (1993); 96. Rubenstein (2007b) 97. Temple (2005); 98. McGowan, Hatchwell & Woodburn (2003); 99. Gaston (1973); 100. Hatchwell et al. (2004); 101.Seddon, Tobias & Butchart (2003); 102. Blackmore & Heinsohn (2007); 103. Eguchi et al. (2007); 104. Brown et al. (1982); 105. Brown & Brown (1981); 106. Williams, Lawton & Lawton (1994); 107. Williams (2000); 108. Williams & Hale (2006); 109. Lawton & Guindon (1981); 110. Caffrey (1999); 111. Caffrey (2000); 112. Magrath (2001); 113. Magrath & Yezerinac (1997); 114. Langen & Vehrencamp (1999); 115. Innes & Johnston (1996); 116. Komdeur (1994); 117. Komdeur (1996); 118. Brouwer et al. 2006); 119. Dickinson, Koenig & Pitelka (1996); 120. Varian-Ramos et al. (2010); 121. Rowley & Russell (1997); 122. Russell & Rowley (1988); 123. Rowley & Russell (1990); 124. Cockburn et al. (2008); 125. Russell et al. (2007); 126. Green et al. (1995); 127. Nias (1986); 128. Nias & Ford (1992); 129. Finn & Hughes (2001); 130. Durrant (2004); 131. Veltman (1989).

Arabian babbler (Turdoides squamiceps)0Yes142–46
Florida scrub-jay (Aphelocoma coerulescens)0YesYesYes247–51
Aapostlebird (Struthidea cinerea)0YesNokNok352
Laughing kookaburra (Dacelo novaeguineae)0Yesh453, 54
Bushtit (Psaltriparus minimus)0Yes555
Sociable weaver (Philetairus socius)0YesNoYes656, 57
White-winged chough (Corcorax melanorhamphos)0YesYesYes758–62
Galapagos hawk (Buteo galapagoensis)0Yes863–65
Acorn woodpecker (Melanerpes formicivorus)0YesYesYesl9, 1066–69
Alpine accentor (Prunella collaris)0Noi1170
Henderson reed warbler (Acrocephalus vaughani taiti)0No1212
Bicolored wren (Campylorhynchus griseus)2YesYesYes1371–73
Dunnock (Prunella modularis)2·2YesNoNo1474–79
Red-cockaded woodpecker (Picoides borealis)2·3YesYesYes15, 1680–84
Stripe-backed wren (Campylorhynchus nuchalis)2·9YesNoNo1773, 85
Whitefronted bee-eater (Merops bullockoides)3·1cYesNoNo1886–90
Purple-crowned fairy-wren (Malurus coronatus)3·8YesYesYes1991
European bee-eater (Merops apiaster)5·3YesYeslYes2092
Carrion crow (Corvus corone)5·6Yes2193
Noisy miner (Manorina melanocephala)5·7Yes2294
Bell miner (Manorina melanophrys)7·7No2395
Superb starling (Lamprotornis superbus)9Yes2496
White-breasted thrasher (Ramphocinclus brachyurus)10Yes2597
Longtailed tit (Aegithalos caudatus)10·5NoNomNo2698–100
Subdesert mesite (Monias benschi)16·7No27101
Grey-crowned babbler (Pomatostomus temporalis)18·3Yes28102–105
Brown jay (Cyanocorax morio)21·6YesNoNo29106–109
American crow (Corvus brachyrhynchos)21·7YeshNoNo30110, 111
Tibetan ground tit (Pseudopodoces humilis)23·4No3131
White-browed scrubwren (Sericornis frontalis)23·5NojNoNo32112, 113
White-throated magpie-jay (Calocitta formosa)39·1NoNoNo33114, 115
Seychelles warbler (Acrocephalus seychellensis)40YesNonNon34116–118
Western bluebird (Sialia Mexicana)43·1YesNoNo35119
Red-backed fairy-wren (Malurus melanocephalus)62·7dNoNo36120
Splendid fairy-wren (Malurus splendens)80·6eNoNoYes37121–123
Superb fairy-wren (Malurus cyaneus)84·4fNoNoYes38–40124–128
Australian magpie (Gymnorhina tibicen dorsalis)85·0gNo41129–131

Effects of subordinates on the benefits of cooperative breeding (increased reproductive success and male and female breeder survival) were compared between species with low (below median, ‘faithful’; 18 species) and high (above median, ‘unfaithful’; 19 species) rates of EGP using a Fisher exact test (Agresti 1992). Effects of subordinates may be similar among species that share common ancestry (Harvey & Pagel 1991). Therefore, phylogenetically informed statistical analyses (generalized least squares models) were also conducted, controlling for phylogenetic associations among species, to examine the link between levels of EGP (as continuous variable) and the benefits of cooperative breeding (whether group size had a positive effect on number of fledglings per nest or breeder survival or not; for a detailed description of the methods, including the phylogeny, see the online Supporting Information).


  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Supporting Information


Clutch size averaged (±SE) 2·9 ± 0·05 eggs, and was unrelated to group size [Table 1(a)]. However, number of fledglings was significantly affected by group size [Table 1(b)]. On average, groups with one subordinate (= 22 nests) produced 0·04 more fledglings per nest than pairs (= 52), whereas groups of four or more (= 24) produced 0·77 more fledglings per nest. Number of fledglings was even more enhanced by number of helpers: number of fledglings per nest increased by 0·42 and 0·92 when pairs had one helper and two or more helpers, respectively [see also Fig. 1a and Table 1(b)].

Table 1.   Overview of benefits of cooperative breeding in Malurus coronatus. Shown are statistical significance and effect sizes for group size and the number of helpers on measures of current productivity [clutch size (a), fledgling production (b)], future productivity [breeder survival (c), re-nesting interval (d)] and total (e) and breeder (f) feeding rates. In models of future productivity (c, d), we also tested for effects of breeder feeding rates. Group size comprises breeders and all subordinates, including individuals that did not contribute to nestling feeding, whereas number of helpers is the number of subordinates that were observed feeding nestlings (see ‘Materials and methods’). Values are obtained from final statistical models after correcting for other significant variables (see ‘Statistical analyses’ in the ‘Materials and methods’ section). Average effect sizes are given (±SE for continuous variables)
 WaldPEffect sizesn
  1. Abbreviations for sample sizes (n) are as follows: c, clutches; p, pairs; n, nests; i, individuals; f, females; w, nest watches; t, territories. Note that sample sizes are smaller in analyses with number of helpers and feeding rates than in analyses with group size, because feeding watches were not conducted on all nests.

(a) Clutch size
 Group size0·120·943: −0·013; 4+: −0·013164 c, 55 p
 Number of helpers0·210·901: −0·025; 2+: −0·00658 c, 43 p
(b) Number of fledglings
 Group size13·470·0023: 0·021; 4+: 0·37398 n, 54 p
 Number of helpers6·730·0471: 0·238; 2+: 0·46050 n, 40 p
(c) Breeder survival
 Group size6·910·0373: 0·906; 4+: 1·94988 i
 Number of helpers3·040·231: 0·798; 2+: 2·10658 i
 Breeder feeding rate8·720·005X ± SE: −0·536 ± 0·18258 i
(d) Re-nesting interval (log-transformed)
 Group size2·460·303: −0·115; 4+: 0·04096 n, 37 f
 Number of helpers1·500·481: −0·029; 2+: 0·16135 n, 22 f
 Breeder feeding rate0·470·50X ± SE: 0·037 ± 0·02435 n, 22 f
(e) Total feeding rate (square-root-transformed)
 Group size4·560·113: 0·001; 4+: 0·284266 w, 73 n, 39 t
 Number of helpers17·33<0·0011: 0·136; 2+: 0·586266 w, 73 n, 39 t
(f) Breeder feeding rate (square-root-transformed)
 Group size23·86<0·0013: −0·343; 4+: −0·386456 w, 70 n, 39 t
 Number of helpers10·520·0011: −0·248; 2+: −0·356456 w, 70 n, 39 t

Figure 1.  Additive effects of helpers on productivity: (a) number of fledglings per nest, and (b) total feeding rates. The graph shows raw data (mean + SE), but statistical analyses controlled for additional variables in (a) generalized linear mixed and (b) restricted maximum likelihood models (see ‘Materials and methods’ section). Numbers depict sample size as: (a) number of nests and (b) number of nest watches, number of nests. Significant differences are indicated at: 5% (*), 1% (**) and 0·1% (***) levels.

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The probability that breeders would survive until a subsequent nest increased from 55% for breeders in pairs, to 75% in groups with one subordinate, and 89% in groups with two or more subordinates [Fig. 2a and Table 1(c)]. The pattern was similar for number of helpers (70%, 84% and 95% survival probability for breeders without, with one helper, and with two or more helpers, respectively), although not significant [Table 1(c)], probably because of lower sample sizes (= 25, 19 and 14 individuals for pairs, groups with one helper and groups with two or more helpers, respectively). Survival probability of breeders until a subsequent nesting attempt was negatively correlated with feeding rate [Fig. 3 and Table 1(c)]. Re-nesting interval was independent of group size, number of helpers and breeder feeding rates [Table 1(d)].


Figure 2.  Compensatory effects of group size on breeders: (a) breeder survival probability until a subsequent nest, and (b) breeder feeding rate. Note that patterns are similar in analyses with ‘number of helpers’ instead of ‘group size’ as independent variable, but for breeder survival the effect is not significant, probably because of small sample size (see Table 1(c)). The graph shows raw data (mean + SE), but statistical analyses controlled for additional variables in (a) generalized linear mixed and (b) restricted maximum likelihood models (see ‘Materials and methods’ section). Numbers depict sample size as: (a) number of birds, (b) number of nest watches, number of nests. Significant differences are indicated at the 5% (*) and 0·1% (***) levels.

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Figure 3.  Average feeding rates at the last or penultimate breeding attempt of breeders that subsequently disappeared and presumably died, or survived, respectively. The graph shows raw data (mean + SE), but statistical analyses controlled for additional variables in (a) generalized linear mixed model (see ‘Materials and methods’ section). Numbers represent number of birds.

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Feeding rates

Nests with two or more helpers received significantly more food than nests of unassisted pairs or pairs with one helper [42% and 30%, respectively; see Fig. 1b and Table 1(e)]. Group size did not significantly affect total feeding rates, although differences between means followed a similar pattern [19% and 18% more feeding trips at nests of groups with two or more subordinates than groups with no or one subordinate, respectively; Table 1(e)]. Male and female breeders in groups fed at lower rates (on average about 20–30% less) than breeders in pairs [Fig. 2b and Table 1(f)], and the effect of number of helpers on breeders’ feeding rate was similar [Table 1(f)].

Comparative study

Subordinates increase productivity (number of fledglings per breeding attempt) in almost all (16 of 18; 89%) faithful species, but only in 9 of the 19 unfaithful species (P = 0·013; see Table 2). Similarly, in the phylogenetic analysis (see online Supporting Information), the effect of subordinates on reproductive success (increase in the number of fledglings per breeding attempt; correlation: −0·189, t37 = −2·454, P = 0·019) is negatively correlated with rates of EGP across species. Thus, subordinates in species with low EGP are more likely to have a positive effect on reproductive success than subordinates in species with high EGP (see Table 2).

In addition, there are clear differences in the enhancement of breeder survival, as survival of assisted male breeders is increased in 7 of 12 (58%) faithful species, but in none of the unfaithful species (P = 0·007; Table 2). Similarly, when correcting for phylogeny, there is a significant negative correlation between probability that subordinates enhance male breeders’ survival and rates of EGP (correlation = −0·232, t21 = −2·353, P = 0·029). A similar pattern is found for enhancement of female survival [analysis of enhancement of female survival in faithful (67%) vs. unfaithful (20%) species; P = 0·043], although this is not statistically significant when correcting for phylogeny (correlation: −0·266, t22 = −1·316, P = 0·20).


  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Supporting Information

Our results show that subordinates contribute substantially to productivity and survival of breeders in M. coronatus. Larger groups fed nestlings at higher rates and produced more fledglings per nest, whereas breeders in groups reduced their work load, resulting in higher survivorship. Benefits of cooperative breeding appear therefore to differ substantially from closely related fairy-wren species. These findings and their implications are discussed in turn in the following.

Benefits of cooperative breeding in Malurus coronatus

Many explanations for the evolution and maintenance of cooperative breeding require a positive effect of subordinate individuals on reproductive success or survival of breeders (Brown 1987; Emlen & Wrege 1989; Cockburn 1998). In general, correlational investigation of effects of subordinates can be problematic (see Cockburn et al. 2008), but several lines of evidence suggest that the positive effects on productivity and survival presented here are a direct result of subordinate contributions: (i) At nests where more than one subordinate assisted, total feeding rates per nest were enhanced, resulting in increased fledgling production (Fig. 1), either through reduced nestling starvation or reduced partial predation associated with nest attendance. (ii) Females did not increase productivity by adjusting clutch size to expected care (e.g. Davies & Hatchwell 1992; Woxvold & Magrath 2005). (iii) Not all subordinates contributed to nestling feeding, and the effect size of number of contributors (helpers) was larger than the effect size of group size [Table 1(b)]. This result suggests that increased fledgling production is a direct result of help with nestling feeding, rather than because of consistently high productivity of certain breeders and/or territories (e.g. Woxvold & Magrath 2005; Cockburn et al. 2008). (iv) Breeders in groups reduced their effort by on average 20–30% compared with breeders in pairs, regardless of the number of subordinates (Fig. 2). If parental care is costly (Bryant 1988; Clutton-Brock 1991; Owens & Bennett 1994; Hatchwell 1999), this reduction in work load is likely to explain the positive correlation between group size and breeder survival (Fig. 2). Indeed, although the relation between number of actual contributors and survival was statistically not significant, probably because of reduced sample sizes, survivorship of male and female breeders was directly negatively related to their own nestling feeding rate at the previous nest (Fig. 3).

If kin selection is the selective force driving the evolution and maintenance of cooperative breeding, subordinates must increase the production of kin. This assumption is fulfilled in M. coronatus, as pair-bonds are long-lasting and extra-pair paternity is rare (4·4% of offspring; Kingma et al. 2009), so in most cases subordinates helped their parents raise their siblings. As subordinates also enhanced productivity (see before), in M. coronatus, kin-selected benefits may arise through increased production of full siblings (Fig. 1) as well as enhanced survival of parents (Fig. 2). Nonetheless, not all subordinates feed nestlings, and not all subordinates are related, so additional benefits for subordinates are possible (see Cockburn 1998): for instance, subordinate individuals may gain future benefits by enhancing group size (Kokko, Johnstone & Clutton-Brock 2001) or by ensuring a higher likelihood of obtaining a breeding position later (Ligon & Ligon 1978). Direct benefits may also play a role in helping behaviour in some cases, as subordinate male M. coronatus can (occasionally) obtain paternity in the nest (Kingma et al. 2009), or subordinates may directly benefit from staying in the territory (Gaston 1978; Kokko, Johnstone & Wright 2002).

The relative importance of compensatory and additive effects

In M. coronatus, patterns of feeding rates correspond to patterns of fledging success (Fig. 1), such that groups with two or more subordinates had higher feeding rates and greater reproductive success (additive effects) compared with pairs and groups with only one subordinate. Surprisingly, breeders reduced their feeding rates (compensatory effects) when accompanied by only one subordinate, thereby equalizing total feeding rate and fledging success. Why would breeders in small groups reduce feeding rates rather than attempt to improve nesting success? It could be that in the long-lived, multi-brooded M. coronatus, breeder investment strategies depend heavily on future reproduction (Trivers 1972; Ghalambor & Martin 2001), rather than on maximizing the outcome of the current brood, in contrast to species that have only one brood per year. It would therefore be interesting to explore whether the relative importance of current and future breeding (including number of annual breeding attempts) correlates with breeder investment strategies among cooperative breeders (see Hatchwell 1999, for such an approach with survival rates and nestling starvation).

Benefits of cooperative breeding: a role for extra-group mating?

The monogamous M. coronatus differs substantially from its promiscuous sister species Malurus melanocephalus, Malurus cyaneus and Malurus splendens in benefits of cooperative breeding. Despite long-term studies, no clear effects of subordinates on fledging success have been reported in these Malurus species. Additionally, male survival, investigated in two of these species, was unaffected by the presence of subordinates (see Table 2 for details). We propose that these interspecific differences may result from differences in investment by subordinates associated with relatedness to the offspring, which is lower in the promiscuous species.

Our comparative analyses of 37 cooperative breeders showed that, similar to the pattern observed among the four fairy-wren species, profound differences in productivity and male breeder survival were associated with levels of extra-group mating (Table 2). These reduced effects of subordinates in cooperatively breeding birds with greater levels of EGP (and hence lower levels of relatedness of subordinates to nestlings), are consistent with the predictions of kin selection theory that subordinates adjust their investment to relatedness of the brood (Hamilton 1964; Komdeur 1996; Emlen 1997; Griffin & West 2003). Future studies that explore whether there are indeed interspecific differences in subordinates investment owing to differences in levels of EGP would therefore be worthwhile.

The question remains why subordinates help in cooperatively breeding species with high rates of EGP. Indeed, the incidence of cooperative breeding in birds declines with increasing levels of extra-pair paternity (Boomsma 2007). Cooperative breeding in promiscuous species may be maintained if direct benefits also play a role (e.g. Richardson, Burke & Komdeur 2002), or subordinates assist minimally to ‘pay-to-stay’ (e.g. Kokko, Johnstone & Wright 2002). Direct benefits for subordinates, in addition or alternative to kin-selected benefits, are therefore interesting to investigate in more detail among cooperatively breeding species, and in promiscuous species particularly.


  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Supporting Information

Our study showed that subordinates simultaneously increase overall productivity and enhance breeder survival in M. coronatus, and that these effects most likely were directly mediated by subordinate individuals’ helping behaviour. Levels of EGP are low, so most subordinates in our population are philopatric offspring of the breeders and full siblings of the nestlings they are caring for. Therefore, indirect inclusive fitness benefits, arising through enhanced productivity of close kin and their parents’ increased survival, may be one reason why subordinate M. coronatus help. Benefits of cooperative breeding are far less clear in the promiscuous fairy-wrens, as in those species subordinates do not affect breeder male survival and nesting success. We showed, based on an extensive review (Table 2), that this pattern is rather general among species. In unfaithful species, the benefits of cooperative breeding are less prevalent than in faithful species, probably because of reduced investment by subordinates associated with lower potential for kin selection. As extra-group mating could significantly alter benefits of cooperative breeding for both breeders and subordinates, incorporating these ideas in the (theoretical) framework of cooperative breeding (Hatchwell 1999), may generate important insights into the evolution and maintenance of the breeding system.


  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Supporting Information

The authors are grateful to Sarah Legge, Steve Murphy and other staff at Mornington Wildlife Sanctuary, and to the Australian Wildlife Conservancy. In addition, they thank their excellent team of field assistants and in particular MSc students Rinskje Klooster and Joppe Rijpstra. Rita Covas and Rob Heinsohn kindly provided unpublished data. Constructive comments from Ben Hatchwell, the editors and an anonymous referee improved the manuscript. This research was funded by the ‘Sonderprogramm zur Förderung hervorragender Wissenschaftlerinnen’ of the Max Planck Society (to A.P.). All fieldwork was performed with permission from the Max Planck Institute for Ornithology Animal Ethics Committee, the Australian Wildlife Conservancy, the Western Australia Department of Conservation and Land Management (licenses BB002178 and BB002311) and the Australian Bird and Bat Banding Scheme (Authority 2230 and 2073).


  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Supporting Information
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Supporting Information

  1. Top of page
  2. Summary
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Conclusions
  8. Acknowledgements
  9. References
  10. Supporting Information

Appendix S1. Methodology of the comparative study among cooperative breeding birds.

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