Family structure and variation in reproductive success in blackbirds

In avian families, some offspring are rendered unequal by parental fiat. By imposing phenotypic handicaps (e.g., via asynchronous hatching) upon certain of their offspring and not others, parents structure the sibship into castes of advantaged “core” offspring and disadvantaged “marginal” offspring that results in an asymmetric sibling rivalry. Here, I show how this family structure scales up to population level reproductive consequences. In a 17-year study of red-winged blackbirds (Agelaius phoeniceus), I show that year-to-year variation in the number of surviving offspring is driven primarily by variation in the number of marginal offspring at hatching and their posthatching survival. Clutch size, core brood at hatching, and fledging varied little from year to year and had little direct effect on year-to-year variation in total brood size at fledging; conversely, variation in the size of the marginal brood at hatching and at fledging was much greater. Marginal but not core brood size at hatching rose with mean clutch size; in years where parents laid larger average clutches they did so by adding marginal progeny. The mean posthatching survival of marginal offspring was always lower than that of core offspring in a given year, and there was no overlap in the distributions. The highest mean survival of marginal offspring across years fell below the lowest mean survival of core offspring; broods were deeply structured. There was an overall female bias among fledglings, and the sex ratio varied across years, with a higher proportion of the smaller female nestlings in years of below average reproductive success. Such variation was especially pronounced in the marginal brood where a higher incidence of brood reduction allowed greater potential for sex-biased nestling mortality. In years of the highest average reproductive success, the sex ratio in the marginal brood approached equality, whereas in years of the lowest average reproductive success, more than two thirds of 8-day-old nestlings were female. Structuring the brood into core and marginal elements allowed parents to modulate both offspring number and sex under ecological uncertainty with direct consequences for population-level reproductive success. They produced fewer and less expensive fledglings in below average years and more and more expensive fledglings in above average years.     

Brood sex ratios, female harem status and resources for nestling provisioning in the great reed warbler (Acrocephalus arundinaceus)

The theory of parental investment and brood sex ratio manipulation predicts that parents should invest in the more costly sex during conditions when resources are abundant. In the polygynous great reed warbler, Acrocephalus arundinaceus, females of primary harem status have more resources for nestling provisioning than secondary females, because polygynous males predominantly assist the primary female whereas the secondary female has to feed her young alone. Sons weigh significantly more than daughters, and are hence likely to be the more costly sex. In the present study, we measured the brood sex ratio when the chicks were 9 days old, i.e. the fledging sex ratio. As expected from theory, we found that female great reed warblers of primary status had a higher proportion of sons in their broods than females of lower (secondary) harem status. This pattern is in accordance with the results from two other species of marsh-nesting polygynous birds, the oriental reed warbler, Acrocephalus orientalis, and the yellow-headed blackbird Xanthocephalus xanthocephalus. As in the oriental reed warbler, we found that great reed warbler males increased their share of parental care as the proportion of sons in the brood increased. We did not find any difference in fitness of sons and daughters raised in primary and secondary nests. The occurrence of adaptive sex ratio manipulations in birds has been questioned, and it is therefore important that three studies of polygynous bird species, including our own, have demonstrated the same pattern of a male-biased offspring sex ratio in primary compared with secondary nests. Received: 1 June 1999 / Received in revised form: 10 January 2000 / Accepted: 12 February 2000     

Paternal expenditure is related to brood sex ratio in polygynous great reed warblers

In many polygynous animals, parents invest more heavily in individual sons than in daughters. However, it is unclear if these differences in investment are a consequence of sex differences in the demand of offspring related to sexual size dimorphism or a consequence of parental manipulation. Here, we report on parental food delivery frequency in relation to brood size and brood sex ratio in a wild population of polygynous great reed warblers Acrocephalus arundinaceus. We used the polymorphic microsatellite loci on the Z chromosome to sex chicks. We found that paternal feeding frequency (times/h per nest) increased not with brood size, but with the proportion of males in the brood, although the demand per nest was more closely related to brood size than to brood sex ratio. Additionally, the increase in rate of paternal feeding frequency in relation to the brood sex ratio was much higher than the increase in rate of nestling food demands. Maternal feeding frequency was independent of both brood size and brood sex ratio. These results strongly suggest that fathers preferentially invest in their sons. We propose that parents can afford sex-biased parental care in animals in which food provisioning is enough for all offspring to survive. Received: 22 January 1996/Accepted after revision: 30 June 1996     

Influences of sex,sex composition of brood and hatching order on mass growth in common terns<Emphasis Type="Italic"> Sterna hirundo</Emphasis>

We studied sex-dependent mass growth of chicks of the monomorphic common tern Sterna hirundo which fledged at a colony site in Wilhelmshaven, Germany, between 1997 and 1999. Brood size, brood mates' sex and hatching order (a-, b- and c-chicks) were known for many individuals, which were sexed by molecular techniques. Daily growth rates and age of fledging were independent of sex. However, in all years male chicks reached higher peak mass and fledged up to 5.2% heavier than female chicks. Broods with at least two fledglings showed that besides sex, brood size interacting with sex composition affected chick mass. In mixed broods, brothers had higher peak and pre-fledging mass than sisters they were reared with. Especially in the combination a-daughter and b-son the brothers were heavier. Lowest mass was found in broods with three nest mates of the same sex. A detailed study of 24 three-fledgling broods showed that male c-chicks were heavier than their siblings. The results reveal an advantage for chicks in mixed broods, especially for sons, and more especially if the son was a c-chick. Higher mass and possibly dominance of sons in c-position might be related to higher maternal androgen levels, which are known to increase with each egg laid. The results suggest that even in a monomorphic species, sons might be more expensive to rear, and are discussed with respect to sibling competition, parental effort, survival of sons, as well as to fitness benefits favoring parents producing sons.     

Sex ratio in lesser black-backed gull in relation to environmental pollutants

In birds, there is ample evidence that the mother can manipulate the sex of the young and produce more of the sex, which gives the highest fitness return. This has previously been documented in gulls, Laridae. Gulls are sexually size dimorphic with males larger than females, and there is good evidence that parents in poor body condition switch their investment to the smallest sex. In the present study, we examined the primary sex ratio and the survival of male and female chicks of lesser black-backed gull (Larus fuscus fuscus) in relation to their blood levels of organochlorines (OCs), perfluorinated compounds (PFCs) and polybrominated diphenyl ethers (BDE-47). We show that females with high levels of OCs (but not PFCs and BDE-47) are likely to skew their sex ratio at hatching towards female offspring. Few females had very high levels of OCs, and the many females with low levels of OCs overproduced sons resulting in a male skew at hatching (59%). The survival of female offspring was lower than the survival of male offspring, causing an even stronger male skew in sex ratio (71%). There is evidence to conclude that circulating levels of OCs in the blood of females may have detrimental effect on the sex allocation strategy and could be of serious threat to the population. Electronic supplementary material  The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

Sex-specific energy requirements in nestlings of an extremely sexually size dimorphic bird, the European sparrowhawk (Accipiter nisus)

Allocation of parental investment is predicted to be equal at the population level between both sexes of offspring, and should lead to sex ratio biases in species that exhibit a sex-difference in parental care. Sex-differences in parental care are rarely quantified. We measured daily energy expenditure in free-living nestlings of the extremely sexually size dimorphic European sparrowhawk (Accipiter nisus), using the doubly labelled water method. These data were combined with measured growth characteristics to estimate daily and total metabolised energy intake of male and female young during the nestling stage. Females reached an asymptotic body mass 1.6 times higher than males. This resulted in a total metabolised energy an estimated 1.4 times higher for the nestling stage. Furthermore, we observed a decline in daily metabolised energy with an increase in brood size, which was significantly stronger for females than for males. These results are discussed in the context of Fishers equal allocation theory. Empirical evidence of a sex ratio bias at the end of parental care, with an overall excess of males, is lacking in this species. Consequently, our data do not support the idea of equal allocation between the sexes. The observed sex difference in daily metabolised energy in response to brood size may give scope for sex ratio bias at the level of the individual brood.     

The influence of parental age and weather on testosterone concentration and offspring survival in broods of tawny owl Strix aluco

Previous research has suggested that parental condition may affect offspring mortality patterns by affecting offspring testosterone levels. Accordingly, we hypothesized that there is a relationship between offspring testosterone concentration and survival during the early nestling period, and that both are influenced by parent age/experience and by prey availability. We tested our hypothesis on tawny owls Strix aluco in their first and third known breeding seasons, when they bred either in adverse or mild weather conditions, in Duna-Ipoly National Park, Hungary. Plasma testosterone concentrations of the nestlings were analyzed and related to parental condition, hatching order and nestling mortality. Inexperienced parents breeding in all weather conditions and experienced parents breeding in adverse conditions were both in poor condition compared to experienced parents breeding in mild conditions. Parents in poor condition produced broods with large between-sibling differences in testosterone concentrations and their later-hatched nestlings (which had low testosterone levels) died during the early nestling period, whereas parents in good condition produced broods with lower variation in offspring testosterone concentrations and all offspring survived the early nestling period. We discuss environmental influences on the amount of testosterone deposited in eggs, and also how maternal testosterone might induce those mechanisms producing testosterone in the nestlings.Communicated by M. Webster, T. Czeschlik     

Offspring reproductive value and nest defense in the magpie (Pica pica)

Summary Magpie (Pica pica) brood defense against a human at the nest was studied in a Mediterranean population with low renesting potential. Variations in two defense measures recorded during 106 trials at 41 different nests were positively correlated with brood age. Ineremental effects due to the number of successive visits to nests by us, brood size, and the time in the breeding season were not significant. Partial correlation analyses showed that visit rate was not an important determinant of nest defense, which thus favors an adaptive explanation of nest defense patterns. Two functional hypotheses to account for the increase in defense intensity with brood age were tested: whether (1) increased parental defense serves to compensate the higher predation risk of older nests or (2) increased parental defense reflects the increasing reproductive value of nestlings as they grow older. Daily mortality and incidende of predation (estimated from contribution of whole-brood losses to total mortality) was higher early in the nestling period, hence providing weak evidence for the assumption on which hypothesis (1) is based. The timing of parental defense intensity did not mirror variations in predation risk for the nest but variations in reproductive value of the brood, as can be estimated from daily mortality, thus supporting hypothesis (2). Magpie parents increased defense intensity in response to premature escaping by almost fully-developed nestlings. Since such a response lowers predation risk for the offspring and increases their probability of survival, this finding supports hypothesis (2), but runs contrary to hypothesis (1). Parents also increased defense in response to play-backs of alarm calls uttered by nestlings during escaping episodes. It is argued that parents should continuously monitor the degree of offspring development in order to assess their reproductive value and that, by alarm calling, chicks honestly make their parents aware of the gain in reproductive value that results from enhancement in locomotory abilities that occur at the end of the nestling period.     

Parental effort in the California gull: tests of parent-offspring conflict theory

Summary Parental effort was studied among knownaged California gulls (Larus californicus) with a brood size of two. Results supported three of Triver's predictions from parent-offspring conflict theory. First, the amount of time parents withheld food from offspring increased with increasing offspring age. Second, older parents were less likely than younger parents to withhold food from offspring throughout the period of parental care. Third, older parents had a longer period of parental care compared to younger parents. Adult survival to future breeding seasons was inversely related to duration of parental care. Older parents, in association with their greater levels of parental effort, had a lower survival rate compared to that of younger parents.     

Age-specific survivorship in relation to clutch size and fledging success in California gulls

Summary Data from a natural population of California gulls (Larus californicus) demonstrated that increasing reproductive effort with age was associated with reduced survivorship. Number of offspring fledged but not clutch size was inversely related to adult survivorhip indicating that reproductively induced mortality resulted from the cumulative effects of the entire breeding season. Agerelated increases in fledging success were correlated with increased adult mortality. Young gulls fledged few offspring and had high survival rates. Old gulls tended to fledge more offspring and had low survival rates. However, those old gulls fledging few offspring survived as well as young gulls. Data also invalidate the assumption that survivorship is age-constant in this species.     

An experimental study of paternal behavior in red-winged blackbirds

Summary The effect of brood size and female nesting status on male parental behavior was investigated in red-winged blackbirds Agelaius phoeniceus using brood size manipulation experiments. Male redwings allocated parental effort on the basis of brood size and nestling age. Males began assisting females only at nests with at least three offspring older than three days. Female nesting status had no singificant influence on male parental care. When females were unable to meet a brood's demand for food, males assisted females with nestling feeding. Females did not reduce the amount of food delivered to nestlings when males assisted. The amount of food brought to nestlings by the male was additional to the amount of food provided by the female. Male assistance increased fledgling success. When female provisioning was sufficient to meet a brood's demand for food males did not assist. The value of male parental care varied inversely with the ability of the female to meet nestling food demands. The ability of unassisted females to provide sufficient food and to raise a brood of nestlings successfully appeared to be influenced by resource abundance.     

Male parental care and monogamy in snow buntings

Summary We experimentally removed males from a random sample of 14 snow bunting (Plectrophenax nivalis) pairs to determine the influence of male parental care on reproductive success. Widowed females increased their rate of food delivery to nestlings by increasing their feeding visit rate but not their load size. However, Widows were only able to achieve 73% of the food delivery rate of Control pairs and, as a result, they raised fewer offspring of lower quality (i.e. lower mass at fledging). Total brood mass raised by Widows was only 55% of that of Control pairs. Thus, in the year of our experiment, male parental care in the nestling period almost doubled the reproductive success realized from a brood. Our experiment, however, was done in a year of poor food availability and data from the previous year, when food supply was higher, indicate that males may not always be so important. Since nestling food supply appears to be unpredictable at the time of pair formation, we suggest that monogamy is a bet-hedging strategy in case of poor food availability. As a consequence the importance of male parental care in some years may explain why snow buntings are almost always monogamous.     

Maternal characteristics and the production and recruitment of sons in the eastern kingbird (<Emphasis Type="BoldItalic">Tyrannus tyrannus</Emphasis>)

Sex allocation theory predicts that if variance in reproductive success differs between the sexes, females who are able to produce high-quality young should bias offspring sex ratio towards the sex with the higher potential reproductive success. We tested the hypothesis that high-quality (i.e., heavy) female eastern kingbirds (Tyrannus tyrannus) that bred early in the breeding season would produce male-biased clutches. A significant opportunity for sexual selection also exists in this socially monogamous but cryptically polygamous species, and we predicted that successful extra-pair (EP) sires would be associated with an excess of male offspring. Although population brood sex ratio did not differ from parity, it increased significantly with female body mass and declined with female breeding date, but was independent of the morphology and display (song) behavior (correlates of reproductive success) of social males and EP sires. Male offspring were significantly heavier than female offspring at fledging. Moreover, the probability that male offspring were resighted in subsequent years declined with breeding date, and was greater in replacement clutches, but lower when clutch size was large. Probability of resighting female offspring varied annually, but was independent of all other variables. Given that variance in reproductive success of male kingbirds is much greater than that of females, and that male offspring are more expensive to produce and have a higher probability of recruitment if fledged early in the season, our results support predictions of sex allocation theory: high-quality (heavy) females breeding when conditions were optimal for male recruitment produced an excess of sons.     

Maternal effects on begging behaviour: an experimental demonstration of the effects of laying sequence, hatch order, nestling sex and brood size

Differential resource allocation by females across the laying sequence has been hypothesised as a mechanism through which females could either compensate nestlings that hatch last in asynchronous broods or promote brood reduction. In this study we artificially incubated eggs and cross-fostered offspring to manipulate nestlings’ position in the hatching order, to identify whether the competitive ability of nestlings is dependent on position in the laying sequence. In both control and experimentally reversed broods, first hatched chicks had a higher survival than last hatched siblings. Yet, nestlings that hatched from eggs laid in the second half of a clutch begged with a greater intensity than nestlings hatched from eggs laid in the first half of a clutch. In natural broods, the greater begging competitiveness of nestlings from later-laid eggs led to a moderation of sibling competition and these nestlings achieved the same body size and weight as nestlings from eggs laid in the first half of the clutch. The lack of a substantial difference in the size and condition of surviving nestlings in respect to laying order suggests that differential resource allocation across the egg-laying sequence partially compensates for hatching last in asynchronous broods and reduces the negative effects of the nestling size hierarchy. The effect of laying order, brood size and experimental treatment also differed for male and female nestlings. Our study highlights the need to be aware of the complex and subtle effects of nestling sex and laying sequence when investigating genetic and environmental influences on individual fitness.     

Brood reduction in response to manipulated brood sizes in the common swift (Apus apus)

Following a brood size manipulation experiment on the common swift (Apus apus) in which different levels of parental effort were created, brood reduction occurred in all five nests manipulated to four chicks and in two of the five manipulated to three young. This provided an opportunity for looking in detail at the parental investment decisions concerning allocation strategies between parent and young during the process of brood reduction. The data recorded here were analysed on a visit-by-visit basis regarding changes in parental and chick body masses, the mass of prey delivered and the estimated mass of parental self-feeding. The results show that food delivery rates did not increase in proportion to the number of chicks in the broods. This reduction in delivery rates per chick resulted in lower chick masses and ultimately in the death of one or more chicks in the larger broods. The resulting low parental body masses for adult birds feeding larger broods suggested that these parents could not have raised all their young without risking their own survival. There was a tendency for parents from nests that experienced brood reduction to feed themselves instead of allocating most of the food gathered to the young. After brood reduction, parents regained lost body mass and their young fledged at masses only slightly lower than normal. The differential allocation decisions regarding parental self-feeding which resulted in brood reduction were largely responsible for keeping the parents in good enough condition to care for the surviving nestlings. Therefore, this study clearly demonstrates that brood reduction can operate through the differential allocation of food between parent and young in a way that can have adaptive consequences for the survival of parents and their young. Correspondence to: T.L.F. Martins     

Patterns of brood division and an absence of behavioral plasticity in a neotropical passerine

Studies of parental behavior in various habitats provide an opportunity to gain insight into how different environments may mold strategies of parental care. Brood division by parents has been hypothesized to occur facultatively within and among species. Brood division occurs when each parent cares for specific offspring within a brood. We studied brood division in a neotropical passerine, the western slaty antshrike (Thamnophilus atrinucha). Our results present a unique picture of a highly specialized example of avian brood division. Division was a fixed behavioral pattern in the population studied: all broods divided by fledging and remained divided during the entire post-fledging period. Brood division before fledging, a previously unreported phenomenon, occurred in 40% of nests observed. Parents that preferentially fed a certain offspring (defined as their focal offspring) in the nest fed the same individual after fledging. Each parent fed only its focal offspring in broods of one and two. The male parent cared for the heavier offspring and the first offspring to leave the nest. Siblings were segregated spatially during the time of highest predation risk. These observations suggest that a consistently high risk of predation on offspring has favored initial spatial segregation and inflexibility of brood division behavior in this species. Factors other than predation risk alone may explain the observed patterns of long-term, perfect brood division. Because high predation is common and relatively predictable in the tropics, selection for fixed brood division may be stronger in tropical birds than in the temperate zone.     

Cooperatively breeding carrion crows adjust offspring sex ratio according to group composition

In cooperatively breeding species, parents should bias offspring sex ratio towards the philopatric sex to obtain new helpers (helper repayment hypothesis). However, philopatric offspring might increase within-group competition for resources (local resource competition hypothesis), diluting the benefits of helper acquisition. Furthermore, benefits of offspring sex bias on parents’ fitness may depend on different costs of production and/or different breeding opportunities of sons and daughters. Because of these counteracting factors, strategies of offspring sex allocation in cooperative species are often difficult to investigate. In carrion crows Corvus corone corone in northern Spain, sons are more philopatric and more helpful at the nest than daughters, which disperse earlier and have higher chances to find a breeding vacancy. Consistent with the helper repayment hypothesis, we found that crows fledged more sons in groups short of subordinate males than in groups with sufficient helper contingent, where daughters were preferred. Crow females also proved able to bias primary sex ratio, allocating offspring sex along the hatching sequence in a way that provided the highest fledging probability to sons in the first breeding attempt and to daughters in the following ones. The higher cost of producing male offspring may explain this pattern, with breeding females shifting to the cheapest sex (female) as a response to the costs generated by previous reproductive attempts. Our results suggest complex adjustments of offspring sex ratio that allowed crows to maximize the value of daughters and sons.     

Experimental increase in food supply influences the outcome of within-family conflicts in Tengmalm’s owl

Within a family there are conflicts of interest between parents and offspring, and between male and female parents, over the supply of parental care. The observed pattern of parental care is the outcome of negotiations within the family, and may be influenced by environmental factors such as food abundance. We experimentally increased food supply to ten Tengmalm’s owl (Aegolius funereus) nests from hatching to fledging, mimicking natural cached prey. Ten un-supplemented nests served as controls. Parents and offspring were fitted with radio-tags. Food provisioning by parents was measured both in the (1) mid- and (2) late nestling stage and in the (3) early and (4) late post-fledging stage. In response to food supplementation, both males and females reduced food provisioning, but the effect was more pronounced in females. Females generally contributed much less to food provisioning than males, and food supplementation increased the difference between the sexes. Mass loss during the brooding stage was substantially lower for supplemented than for control females. Food supplementation did not improve offspring survival, and had no effect on body measurements of nestlings. In conclusion, parents of both sexes used the increased food supply to reduce the costs of caring for their current offspring, but females responded more strongly than males.     

Brood guarding and the evolution of male parental care in burying beetles

Summary Parental behavior that has an impact on the increased survival of offspring, an important factor in the evolution of parental care, can include both guarding and provisioning. The effects of these two components of parental care can be separated and quantified in the burying beetle Nicrophorus orbicollis in which both male and female cooperate to rear young. Although in the absence of competition, reproductive success is reduced by the presence of the second parent in the brood chamber, two parents dramatically reduce the probability that conspecifics will usurp the resource, replace either the male or female, kill the newly hatched brood, and produce a replacement clutch. After the establishment of the burial chamber (but not before) beetles appear to assist their mates in driving off intrasexual competitors. Male assistance in burial does not account for very much of the variance in the speed in which the carcass can be concealed nor are two parents essential to guard against insect predators. There were no significant differences in the duration of parental care by males paired with virgin and non-virgin females suggesting that paternity of the brood for which the male provides care is not a factor determining the length of care. Since male and female reproductive success is limited in Nicrophorus by access to suitable carcasses, many of the typical asymmetries in the costs and benefits of parental care are lacking. However since sperm displacement is not complete, paternity of the replacement clutch, for which the male does not provide care, may be a factor encouraging male desertion before female desertion. Other factors important in the evolution of paternal care, especially the probability of additional reproductive opportunities, are discussed.     

Sex-specific effects of albumen removal and nest environment manipulation on Barn Swallow nestlings

In avian species, maternal provisioning to the eggs is predicted to be more valuable for the offspring under adverse environmental conditions and intense sibling competition. However, studies manipulating both the amount of maternal pre-hatching resources and the harshness of post-hatching environment have seldom been performed to date. In this experimental study of Barn Swallow (Hirundo rustica) nestlings, we tested the consequences of a reduction in the albumen content of the eggs for fitness-related offspring traits, while performing an unbalanced partial cross-fostering soon after hatching, either increasing or decreasing brood size by one nestling. By molecular sexing of the chicks, we additionally tested for sex-specific sensitivity of individual nestlings to experimental treatments and to sex ratio variation in nestmates. We predicted that chicks hatching from albumen-deprived eggs should suffer more than control chicks from the harsher rearing conditions of enlarged broods. However, although albumen removal depressed chick body mass, chicks hatching from control eggs did not fare better than those hatching from eggs with reduced albumen content in enlarged vs. reduced broods. Albumen removal had sex-specific effects on immunity, with males, but not females, hatching from eggs with reduced albumen content showing a lower T-cell-mediated immune response than controls, suggesting that the two sexes were differentially susceptible to resource deprivation during early ontogeny. In addition, both immune response and chick body mass at age 7 days, when maximum growth rate is attained, declined with an increasing proportion of male nestmates. The effect of brood size manipulation on chick body mass at age 12 days, when peak body mass is attained, was also found to depend on brood sex composition, in that an increase in the proportion of male nestmates depressed offspring body mass in reduced broods, while the reverse was true in enlarged broods. On the whole, these findings suggest that sex differences may exist in environmental sensitivity and patterns of resource allocation among different body functions, and that brood size variation and sex composition may affect offspring fitness-related traits.