Males paving the road to polyandry? Parental compensation in a monogamous nesting cuckoo and a classical polyandrous relative

Comparative studies have established the necessity for biparental care as an important factor for monogamy in freshwater fish and birds. However, whether two parents are really needed for offspring care remains an open question in many cases. I experimentally studied female and male contributions to offspring care in the white-browed coucal (Centropus superciliosus), a monogamous and biparental cuckoo with a balanced adult sex ratio, and contrasted it with the sympatric black coucal (C. grillii), a classically polyandrous species with a male-biased adult sex ratio and male-only care. To study the necessity for biparental care, I temporarily removed one partner for 2 days to see whether the remaining parent compensated for the absence of its partner. Both female and male white-browed coucals approximately doubled their feeding rates when their partner was absent, thus fully compensating the number of feeding visits to the nest. However, nestlings maintained their growth only, when males were present and females were removed. When males were removed and only females were present, nestling growth declined. Hence, only male white-browed coucals fully compensated for the temporary loss of the partner, suggesting that females could benefit most from nesting with additional males—if these should become available. Removing female black coucals had no consequence for nestling feeding rates of male black coucals. But male black coucals had to be returned to their territories within a few hours to avoid harming the brood because female black coucals typically would not commence feeding their offspring. In conclusion, the breeding system of white-browed coucals seems quite flexible and the relatively balanced adult sex ratio may stabilize monogamy in this species. Should ecological factors ever favour a stronger bias in the adult sex ratio towards males, female white-browed coucals may easily become polyandrous and relinquish parental care entirely to males.     

Evolution of reversed sex roles, sexual size dimorphism, and mating system in coucals (Centropodidae, Aves)

The evolution of greater male than female parental care remains poorly understood. In birds it is thought to be related to precocial chicks and small clutch size. This review shows, however, that such role reversal has also evolved in a family with altricial young and relatively large clutch size: coucals (Centropodidae, Cuculiformes). Males perform most nest building, incubation, and feeding of young. As predicted by sexual selection theory, coucals have also reversed sexual size dimorphism, females being larger than males in all 12 species for which size data are available. Most coucals that have been studied are monogamous, but the black coucal Centropus grillii appears to be polyandrous, and males perform almost all parental care, whereas females show more active advertisement behaviour. In this species, females are about 50% heavier than males. Polyandry in the black coucal seems to be associated with a shift to a habitat with seasonally rich food resources. Difficulties for female coucals of gathering enough resources for producing several clutches of relatively large eggs may favour mainly male parental care. Female sexual competition and resource storage, and male foraging economy, may explain why females are larger. Additional field studies are needed to test these hypotheses; the coucals are of great interest to sexual selection and mating systems theory.     

Competing Females and Caring Males. Polyandry and Sex-Role Reversal in African Black Coucals, Centropus grillii

Most species of birds show bi‐parental or female‐only care. However, a minority of species is polyandrous and expresses male‐only care. So far, such reversals in sex roles have been demonstrated only in precocial bird species, but there was suggestive evidence that such a mating system may occur in one altricial bird species, the black coucal, Centropus grillii. In a field study in Tanzania we investigated whether black coucals are sex‐role reversed and polyandrous. We found that males were mated to one female, rarely vocalized and provided all parental care from incubation of eggs to feeding of young. In contrast, female black coucals were about 69% heavier and 39% larger than males and polyandrous. They spent a large proportion of time calling from conspicuous perches, defended breeding territories, did not help in provisioning young and had a higher potential reproductive rate than males. We conclude that the black coucal currently represents the only altricial bird species with sole male parental care and a classical polyandrous mating system. High nest predation pressure and small territory sizes due to high food abundance may have been important factors in the evolution of sex‐role reversal and polyandry in this species.     

Competing females and caring males. Sex steroids in African black coucals, Centropus grillii

The black coucal is the only known altricial bird species in which females mate with and lay eggs for more than one male and males are responsible for all parental care (classical polyandry). In this species, the left testis is atrophied and it has been speculated that this may result in a reduction of circulating androgens, providing a unique mechanism for reversals in sex roles. We therefore investigated whether there is a reversal in circulating androgens and oestrogens in black coucals. Despite the reversals in sex roles, males had significantly higher levels of plasma testosterone than females, in a pattern typical of that of monogamous male passerines. Testosterone levels of both sexes were higher during the mating than during the premating stage and were low in males during the nestling stage. The concentrations of androstenedione, dehydroepiandrosterone and oestradiol did not differ between the sexes and were generally low. A physiological challenge with gonadotropin-releasing hormone (GnRH) resulted in a significant increase in testosterone in males but not in females, suggesting either that females are not responsive to GnRH or that they express patterns of testosterone that are similar to those of males of species with a polygynous mating system without paternal care, in which testosterone is expressed at maximum levels throughout the breeding season. We conclude that the absence of one testis does not provide a mechanism for sex role reversal in black coucals. Either androgens are not involved in the regulation of male-like traits in females or females are sensitive to relatively low levels of these steroids.     

Social monogamy vs. polyandry: ecological factors associated with sex roles in two closely related birds within the same habitat

Why mainly males compete and females take a larger share in parental care remains an exciting question in evolutionary biology. Role‐reversed species are of particular interest, because such ‘exceptions’ help to test the rule. Using mating systems theory as a framework, we compared the reproductive ecology of the two most contrasting coucals with regard to sexual dimorphism and parental care: the black coucal with male‐only care and the biparental white‐browed coucal. Both species occur in the same lush habitat and face similar ecological conditions, but drastically differ in mating system and sexual dimorphism. Black coucals were migratory and occurred at high breeding densities. With females being obligatory polyandrous and almost twice as heavy as males, black coucals belong to the most extreme vertebrates with reversed sexual dimorphism. Higher variance in reproductive success in fiercely competing females suggests that sexual selection is stronger in females than in males. In contrast, resident white‐browed coucals bred at low densities and invariably in pairs. They were almost monomorphic and the variance in reproductive success was similar between the sexes. Black coucals were more likely to lose nests than white‐browed coucals, probably facilitating female emancipation of parental care in black coucals. We propose that a combination of high food abundance, high population density, high degree of nest loss and male bias in the adult sex ratio represent ecological conditions that facilitate role reversal and polyandry in coucals and terrestrial vertebrates in general.     

Long-term consequences of early ontogeny in free-living Great Tits Parus major

Environmental factors during early development may have profound effects on subsequent life-history traits in many bird species. In wild birds, sex-specific effects of early ontogeny on natal dispersal and future reproduction are not well understood. The objective of this work was to determine whether hatching date and pre-fledging mass and condition of free-living Great Tits Parus major have any subsequent effect on individuals’ natal dispersal and reproductive performance at first breeding. Both males and females dispersed longer distances in coniferous than in deciduous forests, while dispersal was condition-dependent only in males (heavier as nestlings dispersed farther). In females, mass and condition at pre-fledging stage correlated significantly with clutch size, but not with subsequent reproductive performance as measured by fledging success or offspring quality. In contrast, heavier males as nestlings had higher future fledging success and heavier offspring in their broods compared with those in worse condition as nestlings. The hatching date of female as well as male parents was the only parental parameter related to the number of eggs hatched at first breeding. These results indicate that pre-fledging mass and condition predict subsequent fitness components in this bird species. We suggest that sex-specific relationships between a disperser’s condition and its selectivity with respect to breeding habitat and subsequent performance need to be considered in future models of life-history evolution.     

Who Cares? Males Provide Most Parental Care in a Monogamous Nesting Cuckoo

Cuckoos hold a prominent position in the study of parental care, because they show the greatest variation of any bird family in the way they care for their offspring. Despite this, few data are available on cuckoos with biparental care even though it is the most common form of parental care in cuckoos and birds in general. Here I describe the breeding behaviour of the pheasant coucal, Centropus phasianinus , an old-world nesting cuckoo. I show that males almost exclusively build the nest and incubate and brood the young alone both at night and during the day. The incubation pattern of short, c . 40 min bouts on the nest interspersed with 20 min frequent recesses is well suited to incubation by a single parent and is widespread amongst birds. Males also defend the nestlings and deliver 80% of the feeds to the young consisting of insects (65%), frogs and reptiles. Females did not compensate for their fewer feeding visits by delivering more vertebrates than males. Although coucal males get little help feeding, the hourly feeding rate of 3.8 feeds per brood (1.4 feeds/nestling) exceed that of the few nesting cuckoos studied to date and matches that of other tropical non-passerines. Predominantly male care is found in less than 5% of birds, mainly species with reversed sexual size dimorphism or reversed sex-roles. Its evolution, especially in monogamous species, remains puzzling. The breeding behaviour of pheasant coucals illustrates a possible transitional stage in the evolution of polyandry and interspecific brood parasitism in cuckoos.     

Front Cover

In most animals, competition for mating opportunities is higher among males, whereas females are more likely to provide parental care. In few species, though, these "conventional" sex roles are reversed such that females compete more strongly for matings and males provide most or all parental care. This "reversal" in sex roles is often combined with classical polyandry—a mating system in which a female forms a harem with several males. Here, we review the major hypotheses relating such role reversals to evolutionary and behavioural traits (anisogamy, phylogenetic history, sexy males, parental care, genetic paternity, trade‐off between mating and parenting, adult sex ratio) and to ecological factors (food supply, offspring predation). We evaluate each hypothesis in relation to coucals (Centropodinae), a group of nesting cuckoos of great interest for mating system and parental care theory. The black coucal (Centropus grillii) is the only known bird combining classical polyandry with altricial development of young, a costly trait with regard to parental care. Our long‐term study offers a unique possibility to compare the strongly polyandrous black coucal with a monogamous close relative breeding in the same area and habitat, the white‐browed coucal (C. superciliosus). We show that the evolution of sex roles in coucals and other animals has many different facets. Whereas phylogenetic constraints are important, confidence in genetic paternity is not. In combination with facilitating ecological conditions, adult sex ratios are key to understanding sex roles in coucals, shorebirds, and most likely also other animals. We plead for more studies including experimental tests to understand how biased adult sex ratios emerge and whether they drive sexual selection or vice versa. How do sex ratios and sexual selection interact and feedback on each other? Answers to these questions will be fundamental for understanding the evolution of sex roles in mating and parenting in coucals and other species.     

Behavioural responses to ectoparasites in pied flycatchers Ficedula hypoleuca: an experimental study

Nests of cavity‐nesting birds usually harbor some species of haematophagous ectoparasites that feed on the incubating adults and nestlings. Given the negative impact of ectoparasites on nestlings there will be selection on hosts to reduce parasite infestations through behavioural means. We have experimentally reduced the abundance of all ectoparasites in nests of pied flycatchers Ficedula hypoleuca to explore both whether there are changes in the frequency and duration of putative anti‐parasite behaviours by tending adults, as well as whether such anti‐parasite behaviours are able to compensate for the deleterious effects that parasites may have on nestlings. Heat treatment of nests substantially decreased the density of ectoparasites, and thereby positively affected nestling growth. The frequency and intensity of female grooming and nest sanitation behaviours during the incubation and nestling periods decreased as a consequence of the experimental reduction of ectoparasite infestation. Although nestlings begged more intensely in infested nests, the experiment had no significant effect on parental provisioning effort. Reduction of parasites resulted in larger nestlings shortly before fledging and increased fledging success. This study shows a clear effect of a complete natural nest ectoparasite fauna on parental behaviour at the nest and nestling growth in a cavity‐nesting bird. Although ectoparasites induce anti‐parasite behaviours in females, these behaviours are not able to fully remove parasite's deleterious effects on nestling growth and survival.     

Development of intraspecific size variation in black coucals,white-browed coucals and ruffs from hatching to fledging

Most studies on sexual size dimorphism address proximate and functional questions related to adults, but sexual size dimorphism usually develops during ontogeny and developmental trajectories of sexual size dimorphism are poorly understood. We studied three bird species with variation in adult sexual size dimorphism: black coucals (females 69% heavier than males), white-browed coucals (females 13% heavier than males) and ruffs (males 70% heavier than females). Using a flexible Bayesian generalized additive model framework (GAMM), we examined when and how sexual size dimorphism developed in body mass, tarsus length and bill length from hatching until fledging. In ruffs, we additionally examined the development of intrasexual size variation among three morphs (Independents, Satellites and Faeders), which creates another level of variation in adult size of males and females. We found that 27–100% of the adult inter- and intrasexual size variation developed until fledging although none of the species completed growth during the observational period. In general, the larger sex/morph grew more quickly and reached its maximal absolute growth rate later than the smaller sex/morph. However, when the daily increase in body mass was modelled as a proportion, growth patterns were synchronized between and within sexes. Growth broadly followed sigmoidal asymptotic models, however only with the flexible GAMM approach, residual distributions were homogeneous over the entire observation periods. These results provide a platform for future studies to relate variation in growth to selective pressures and proximate mechanisms in these three species, and they highlight the advantage of using a flexible model approach for examining growth variation during ontogeny.     

Unusual pattern of sex‐specific mortality in relation to initial brood sex composition in the black‐billed magpie Pica pica

In sexually size‐dimorphic species, brood sex composition may exert differential effects on sex‐specific mortality. We investigated the sex‐specific mortality and body condition in relation to brood sex composition in nestlings of the black‐billed magpie Pica pica. Neither significantly sex‐biased production at hatching nor overall sex‐biased mortality during the nestling period was found. Sex‐specific mortality as a function of brood sex composition, however, differed between female and male nestlings. We found higher mortality for females in male‐biased broods and higher mortality for males in female‐biased broods, a phenomenon that we call ‘rarer‐sex disadvantage’. As a result, fledging sex ratios became more biased in the direction of bias at hatching, a phenomenon that cannot be readily explained by previous hypotheses for sex‐specific mortality. Two temporal variables, fledging date and laying date, were also correlated with sex‐specific mortality: female nestlings in earlier broods experienced higher mortality than male nestlings whereas male nestlings in later broods experienced higher mortality. We suggest that this unusual pattern of mortality may be explained by adaptive adjustments of brood sex composition by parents, either through the effects of a slight sex difference in offspring dispersal patterns on parental fitness, or owing to sex differences as regards the benefits of early fledging.     

The effect of parental quality and malaria infection on nestling performance in the Collared Flycatcher (Ficedula albicollis)

Plumage ornamentation often signals the quality of males and, therefore, female birds may choose elaborately ornamented mates to increase their fitness. Such mate choice may confer both direct and indirect benefits to the offspring. Males with elaborate ornaments may provide good genes, which can result in better nestling growth, survival or resistance against parasitic infections. However, these males may also provision their offspring with more food or food of better quality, resulting in nestlings growing at a higher rate or fledging in better condition. In this study, we examined if there was an association between male ornamentation and malaria infection in Collared Flycatchers (Ficedula albicollis). We also investigated offspring performance in relation to malaria infection in the parents and the quality of the genetic and rearing fathers (assessed by the size of two secondary sexual characters) under simulated good and bad conditions (using brood size manipulation). We found that secondary sexual characters did not signal the ability of males to avoid parasitic infections, and malaria infection in the genetic and the rearing parents had no effect on nestling growth and fledging size. Our results do show, however, that it may be beneficial for the females to mate with males with a large forehead patch because wing feathers of nestlings reared by large-patched males grew at a higher rate. Fast feather growth can result in earlier fledging which, in turn, could improve nestling survival in highly variable environments or under strong nest predation.     

Sexual differences in moult–breeding overlap and female reproductive costs in pied flycatchers, Ficedula hypoleuca

1. In this study I show that a sexual difference in timing of the post-nuptial moult frequently occurs in a sub-arctic population of the pied flycatcher.
2. Most pairs started to moult after fledging of their young, but an overlap between moult and nestling feeding was more common among males than females. This sexual difference in moult–breeding overlap increased as the season progressed.
3. Females with moult–breeding overlap laid smaller clutches than non-moulting females. In addition to many other factors explaining the seasonal decline in clutch size that has been found for many bird species, it is possible that females adjust their clutch size according to their own risk of having to start moulting while still feeding the nestlings.
4. Nearly 24% of the females were deserted by their mate before the young fledged. Desertion imposed no fitness costs to males in terms of fledgling number or quality, suggesting that their females managed to adjust their care for the loss of male care.
5. Deserted females started moulting later than aided females, which may be a result of their increased reproductive investment.
6. Deserted females and females aided by moulting males had lower survival rate than females aided by non-moulting males.
7. These findings suggests that delayed moult may be one mechanism causing inter-annual reproductive costs in birds, and the relationship between a sexual difference in timing of moult and its fitness consequences may be widespread among passerine birds.     

Growth and morphology of nestling Hooded crows Corvus corone cornix, a sexually dimorphic bird species

The growth and morphology of nestling Hooded crows, Corvus corone cornix , were studied at Trondheim, Central Norway, during 1980 and 1981. The sexual size dimorphism of the nestlings developed while they were in the nest, but was less pronounced than that of the juvenile birds. Female young grew relatively faster than the males. The size variation of the morphological characters studied was greater in the males than in the females, during the entire nestling period. The order of development of the different morphological characters seemed to be adapted to the needs of the nestlings during the nestling period. Growth of the bone and bill characters was the highest priority, body weight and feather characters the lowest. In general, the sizes of the different morphological characters were highly intercorrelated, particularly those that developed at the same time during the growth period. In the favourable breeding season of 1981, the nestlings were larger than in the unfavourable season of 1980. The high priority characters of the males increased more in size than did those of the females, and the low priority characters of the females increased more in size than did those of the males. About 75% of the nestlings could be correctly sexed from their external morphological characteristics. The findings support the view that the parental cost of rearing a male offspring is greater than that of a female.     

Brood provisioning rates and fledgling behavior of Cordilleran Flycatchers in southwestern Colorado

The behavior of young songbirds after fledging is one of the least understood phases of the breeding cycle, although parental provisioning rates and movement of fledglings are key to understanding life history evolution. We studied Cordilleran Flycatchers (Empidonax occidentalis) at two sites in southwestern Colorado, USA, from 2012 to 2017. We banded and sexed breeding adults to determine the relative contributions of males and females to nestling and fledgling care, and attached radio‐transmitters to nestlings to facilitate observations of brood behavior after fledging. Females made 60% and 78% of total observed feedings of nestlings and fledglings, respectively. Parental provisioning rates increased with nestling age, and per‐nestling provisioning rates increased with brood size. Parental provisioning rates declined just before fledging, then increased just after fledging. Fledging times of individuals in broods were asynchronous and concentrated during the late afternoon and early evening. Males stopped caring for fledglings before females even though this species is single‐brooded, with some late‐season broods being abandoned by males. Broods spent the first three weeks after fledging within 400 m of nests, after which they began to disperse. Most aspects of the breeding biology of Cordilleran Flycatchers in our study, including the duration of nestling and fledging periods, female‐dominated provisioning, and movement patterns of fledglings, were similar to those of other Empidonax species. However, the times when young fledged were not concentrated in the morning as reported in most other songbirds, and this result warrants additional study of the timing of fledging in ecologically and taxonomically similar species. The increased per‐nestling provisioning rate with increasing brood size was unexpected, and additional study is needed to determine if this increase results from a trade‐off between adult annual survival and productivity favoring increased provisioning of young in larger broods, or from the existence of high‐quality individuals where larger clutches and higher provisioning rates are linked.     

Effect of altitude on male parental expenditure in Mountain Bluebirds ( Sialia currucoides ): are higher-altitude males more attentive fathers?

Male investment of time and energy in caring for offspring varies substantially both between and within bird species. Explaining this variation is of long-standing interest to ornithologists. One factor that may affect male care is breeding site altitude, through its effects on climate. The harsher, less predictable abiotic conditions at higher altitudes are hypothesized to favour increased male investment of time and energy in offspring care. We tested this hypothesis by comparing male parental behaviour in Mountain Bluebirds (Sialia currucoides) nesting at 1500 and 2500 m a.s.l. in the Bighorn Mountains of Wyoming, USA. We compared rates of prey delivery to nestlings at these two altitudes at two times: 1–2 days after hatching, when females spend much of their time brooding young, and 12–13 days later, when brooding has ended and nestling energy demands are peaking. High-altitude males fed nestlings 18 and 28% more often than low-altitude males early and later in the nestling stage, respectively, but only the difference in late-stage feeding rates were significant. Like males, females at the high site also fed nestlings significantly more often than females at the low site later in the nestling stage (45% difference in feeding rates). Consequently, the proportion of all feeding trips made by males at the high site (40%) did not differ significantly from that at the low site (44%). Parents at the high altitude may feed nestlings more often to compensate for their greater thermoregulatory costs. Parents may also be attempting to assist nestlings in storing fat and/or attaining a large size and effective homeothermy as quickly as possible to enhance nestling ability to survive bouts of severe weather which are common at high altitudes.     

Philornis infection in blue‐black grassquits: impact on nestlings and risk factors involved

Parasitic botfly larvae (Philornis ssp., Diptera: Muscidae) are found in nests of several bird taxa, although prevalence and impact on nestling survival vary considerably among species. Here we describe patterns of botfly infestation in blue‐black grassquit Volatinia jacarina nestlings. We identified the most typically affected nestling body parts and assessed parasite prevalence, impact on nestling survival, and changes in nestling body shape. Additionally, we tested whether climatic conditions, nest morphology and habitat characteristics are associated with larvae abundance. Blue‐black grassquits had low breeding success (16% of eggs/nestlings survived to fledged; 19% of the nests fledged at least one), but most failures resulted from predation by vertebrate predators. We estimated that 1% of nestlings died due to botfly infestation, and the number of subcutaneous larvae (range 1–18) in a nestling's body did not predict fledging success. Infected chicks exhibited higher tarsus asymmetry. Thus, we argue that although botflies had a small impact on offspring survival, they may reduce fitness in adulthood. There was no evidence that environmental conditions and nest morphology are linked to the number of larvae on nestlings. Nesting areas with higher food supply had lower infestation rates. Possibly, food‐rich habitats allow parents to invest more time in offspring care (brooding nestlings), thus protecting them from fly attacks. Alternatively, vegetation composition could influence local invertebrate diversity, which could provide a natural trophic buffer against adult Philornis. The present study brings to light new perspectives concerning bird–botfly interaction.     

Behavior of adult and young grassland songbirds at fledging

The behavior of adults and young at the time of fledging is one of the least understood aspects of the breeding ecology of birds. Current hypotheses propose that fledging occurs either as a result of parent‐offspring conflict or nestling choice. We used video recordings to monitor the behavior of nestling and adult grassland songbirds at the time of fledging. We observed 525 nestlings from 166 nests of 15 bird species nesting in grasslands of Alberta, Canada, and Wisconsin, USA. Overall, 78% of nestlings used terrestrial locomotion for fledging and 22% used wing‐assisted locomotion. Species varied in propensity for using wing‐assisted locomotion when fledging, with nestling Grasshopper Sparrows (Ammodramus savannarum) and Henslow's Sparrows (Centronyx henslowii) often doing so (47% of fledgings) and nestling Song Sparrows (Melospiza melodia), Common Yellowthroats (Geothlypis trichas), and Chestnut‐collared Longspurs (Calcarius ornatus) rarely doing so (3.5% of fledgings). For 390 fledging events at 127 nests, camera placement allowed adults near nests to be observed. Of these, most young fledged (81.5%) when no adult was present at nests. Of 72 fledging events that occurred when an adult was either at or approaching a nest, 49 (68.1%) involved feeding. Of those 49 fledgings, 30 (62.1%) occurred when one or more nestlings jumped or ran from nests to be fed as an adult approached nests. The low probability of nestlings fledging while an adult was at nests, and the tendency of young to jump or run from nests when adults did approach nests with food minimize opportunities for parents to withhold food to motivate nestlings to fledge. These results suggest that the nestling choice hypothesis best explains fledging by nestlings of ground‐nesting grassland songbirds, and fledging results in families shifting from being place‐based to being mobile and spatially dispersed.     

Age‐related prenatal maternal effects and postnatal breeding experience have different influences on nestling development in an altricial passerine

Reproductive success and nestling performance are related to the age of parents across several vertebrate taxa. However, because breeding experience and prenatal maternal investment in reproduction often covary, the source of these age‐related differences can be difficult to determine. In this study, we evaluated the influence of prenatal maternal effects and postnatal breeding experience on the performance of nestling tree swallows Tachycineta bicolor by conducting a carefully controlled partial cross‐fostering experiment. We swapped half‐broods of nestlings between the nest of a young first‐time breeding female and the nest of a female known to have previously raised and fledged young. Our manipulation did not influence the within‐brood nestling hierarchies, and controlled for the effects of egg laying order. We found that nestlings of older females were heavier just prior to fledging regardless of the breeding experience of the attending female. In addition, fledglings raised by experienced females grew their flight feathers faster, and had greater probability of fledging. Our study demonstrates that prenatal investment in reproduction by older females can have long‐term consequences on nestling mass, and suggests limited potential for compensatory mass gains prior to fledging. Because our analyses controlled for feeding rates, our results also suggest that foraging quantity and quality are not the only benefits nestlings gain by being raised by an experienced female.