Statistical models of annual reproductive success in the cooperatively breeding superb fairy-wren Malurus cyaneus identified three strong positive correlates: spring rainfall, the age of the breeding female, and the presence of supernumeraries on the territory. However, analysis of changes within females suggest that while the effect of female age is causative, the effect of help by supernumeraries is not. Instead, high-quality breeders and/or territories are likely to accumulate philopatric supernumeraries. However, supernumeraries do provide a deferred benefit, increased likelihood that the breeding female will survive to breed again. This effect is likely to be causative because increased survival is not observed in the philopatric sex, contrary to predictions of the hypothesis that characteristics of the territory rather than help per se promote survival.
Statistical models suggest that reproductive success is correlated with spring rainfall, an increase in age, and the presence of at least one supernumerary. The effect of rainfall is easily understood in this case. The study periods encompassed some of the most severe drought conditions recorded in south-eastern Australia, and these clearly restricted virtually every aspect of the reproduction of the fairy-wrens, almost certainly by reducing the availability of food.
Three hypotheses are commonly invoked to explain age-related increases in reproductive success in birds (Curio 1983; Saether 1990; Forslund & Pärt 1995). First, some aspect of parental skill could increase with experience or maturation, such as foraging ability and habitat selection (e.g. Pärt 2001), or co-ordination with other group members (Nevoux, Weimerskirch & Barbraud 2007). Second, because the residual reproductive success of birds declines with age, increased risk-taking may be favoured as age advances, though this could be countered if low-quality individuals incur fewer reproductive costs (e.g. Pärt, Gustafsson & Moreno 1992). Finally, the elimination of low-quality individuals through selection may lead to homogeneous high-quality individuals at advanced ages (e.g. Cam & Monnat 2000; Mauck, Huntington & Grubb 2004). The latter hypothesis is not supported in this case, as first year females that survived to breed again had similar productivity to those that did not, and individual females on average increased their success by 50% from year to year. Hence the effect of age is likely to be causative.
The residual reproductive success hypothesis does not predict that the effects of age will be concentrated between the first and second year of life in birds that can breed for nine breeding seasons. Hence, some aspect of experience is implicated. The absence of an interaction between rainfall and breeding output contrasts with several studies that have reported the poor performance of young birds is exacerbated by severe environmental conditions (e.g. Laaksonen, Korpimäki & Hakkarainen 2002; Bunce, Ward & Norman 2005). This suggests that foraging ability may be less important in determining differences between first and older birds than experience at nest location and construction, as vulnerability to predators may be a more important determinant of output than foraging ability (e.g. Komdeur 1996). None the less, birds of all ages gain a considerable advantage from improved rainfall (Fig. 5).
Our analyses of the consequences of help are more complicated. The initial statistical modelling revealed a positive association between help and productivity, while paired comparisons of females with and without help suggest that this is not due to help per se. In addition, the productivity of birds influences the likelihood that helper numbers will change (Fig. 4b), as predicted by both the Dickinson–Hatchwell conjecture and the hypothesis that high-quality territories will be more likely to recruit supernumeraries. Can these alternatives be distinguished? Dickinson & Hatchwell (2004) have argued the association between productivity and the likelihood that helper number will change precludes the use of paired comparisons to control for female/territory effects of help. However, their underlying logic is not clear, as detection of an effect of help is only impossible if there are some individuals that are so superior that they derive no further benefit from help, and another subclass that are so poor that they would gain no benefit from help. Indeed, a logical corollary is that if large proportions of birds undergo changes in group size, as occurs in our data (129 of 223; 57%), the population would eventually reorganize so that birds with supernumeraries would gain no benefit from their presence, while birds that were incompetent at reproduction would be unassisted. This of course exacerbates the unreliability of mean values, and hence reduces even further the ability to interpret the correlations detected in the statistical models as causative. It is less clear that paired comparisons are undermined. For example, in the fairy-wren data, the Decreaser class has intermediate productivity to the Neither or Both class (Fig. 4). It could be argued that Both–Decreaser equals the component due to environmental/female quality, and Decreaser–Neither equals the effect attributable to help. Hence, we predict further decline equivalent to Decreaser–Neither once the helper is no longer present, but there is no change in our data (Fig. 4).
In addition, the Dickinson–Hatchwell argument trivializes the complex process of acquisition and loss of supernumeraries. Loss can occur on successful territories because death or dispersal to neighbouring vacancies outweighs recruitment. In turn, recruitment depends not just on productivity, but on production of the philopatric sex, which is not guaranteed because the number of independent young is so low that often only daughters will be reared. By contrast, in M. cyaneus an increase in the number of supernumeraries is most likely for (1) older females, which have greater productivity, and hence more likely to recruit helpers than 1 year olds, and (2) when drought breaks, when reproductive success increases sharply. It is because helper number increases after rain that the productivity of Increasers exceeds that for the Both class. However, despite the high productivity of Increasers, there is no evidence of a production threshold, as their average performance is less than rearing a single brood to independence. Hence, a further effect of help should be detectable, but does not occur. Thus while dissection into the four classes envisaged by the Dickinson–Hatchwell conjecture is a useful step in analysis, we do not believe their argument that the paired comparison method will not reveal helper effects if they are present. In the case of M. cyaneus, there is no evidence that acquisition or loss of a supernumerary leads to gain or reduction in productivity, so we argue that the correlation between group size and productivity is likely to be a consequence of greater recruitment of supernumeraries where the quality of the territory or female is high. However, it will prove interesting to apply these methods to examine the situation in other species where the relativities between the four classes are different, as this may allow novel insights.
By contrast, our analyses reveal a hitherto unreported correlation between the presence of supernumeraries and the subsequent survival of the female. Effects of helpers on future reproductive success are plausible, as many cooperative breeders use the presence of helpers to reduce the amount of parental care (load-lightening), rather than increase productivity (Hatchwell 1999). This is particularly true where nestling starvation is rare (Hatchwell 1999), as in the case in fairy-wrens. However, detecting effects on survival is notoriously difficult to interpret, as load-lightening could lead to improved survival, but territories where survival is enhanced should also accumulate philopatric helpers. Alternative approaches are difficult, as paired comparisons are confounded where death is one of the outcomes, and experiments that increase mortality are questionable ethically. There is also the possibility that highly localized density-dependent competition between group members could cause reduced survival (Cockburn et al. 2003; Brouwer et al. 2006). However, because we have detected enhanced survival in females, which are never philopatric, and no benefit for males, the philopatric sex, we believe that our results are best interpreted as evidence of a causative improvement of survival.
The fact that females rather than dominant males gain a survival benefit is surprising, because dominant males reduce provisioning in the presence of a helper more than females (Dunn & Cockburn 1996). Our earlier analyses had suggested that males may use load-lightening to increase the rate of extra-group courtship displays (Green et al. 1995). However, subsequent work revealed that additional courtship during the breeding season is unlikely to increase extra-group parentage (Green et al. 2000), which instead is based on courtship outside the period of parental provisioning (Dunn & Cockburn 1999; Double & Cockburn 2003).
A possible reason for the greater sensitivity of female survival is that males provision at a much lower rate than they can potentially achieve (MacGregor & Cockburn 2002), and are largely insensitive to the needs of the brood (Dunn & Cockburn 1996). By contrast, female provisioning responds strongly to brood size and nestling age (Dunn & Cockburn 1996), and it may be the costs of this sensitivity that allows females to benefit from load-lightening. However, it is more likely that the difference arises because females are exclusively responsible for some components of investment, and hence the unique beneficiaries of any reduction in those components. In particular, females reduce the size of the eggs they lay when they have helpers, yet this reduced investment is fully compensated by the increased food delivery that occurs at nests with helpers (Russell et al. 2007). Females thus use helpers to obtain future benefits rather than to enhance current reproductive benefits.
These analyses exacerbate the paradox posed by the balance between cost and benefits experienced by dominant male fairy-wrens that tolerate helpers. Our previous work has identified three severe costs to dominant males of the presence of a supernumerary. Females with helpers increase the allocation of paternity to extra-group males, so the addition of a single helper reduces within-group paternity (Mulder et al. 1994; Dunn & Cockburn 1999). In addition, females are often unrelated to the supernumerary males, and in these circumstances allow the supernumerary about one-quarter of the young that are sired within-group (Cockburn et al. 2003). Third, if the dominant male is sufficiently attractive to solicit visits from extra-group females, he is vulnerable to parasitism by the helper (Double & Cockburn 2003). The results we report here suggest that these costs are not compensated by increased fecundity or survival. In dramatic contrast, the female gains two substantial benefits from the presence of helpers. First, constraints on unrestricted mate choice are alleviated, so she is free to allocate paternity among a large pool of potential sires (Mulder et al. 1994). Second, females without helpers have a 50% greater chance of death between breeding seasons compared with those that were assisted by a supernumerary.
Collectively, these observations raise the problem of why males tolerate helpers. The absence of female supernumeraries is in part a consequence of aggression by the dominant female, suggesting expulsion of supernumeraries is feasible. Why this does not occur is perhaps the greatest unresolved problem in understanding the remarkable social and mating system of these birds.