Seasonal decline of offspring quality in the European starling Sturnus vulgaris: an immune challenge experiment

In seasonally fluctuating environments, timing of reproduction is a crucial determinant of fitness. Studies of birds show that late breeding attempts generally result in offspring of lower reproductive value, with lower recruitment and long-term survival prospects. Several proximate mechanisms, including a seasonal decline of immune system functioning, may lead to a seasonal decline of offspring fitness. We investigated seasonal variation in offspring quality by subjecting first- and second-brood chicks of a sexually size dimorphic species, the European starling Sturnus vulgaris, to an immune challenge with a bacterial endotoxin (LPS), and evaluated their growth and physiological response in terms of total plasma antioxidant capacity (TAC), concentration of reactive oxygen metabolites and hematocrit. LPS challenge did not affect chick growth or oxidative status. However, hematocrit of second-brood chicks was higher in LPS chicks compared to controls. Body mass halfway through the rearing period (days?8–9 post-hatching), TAC and hematocrit were lower among second- vs. first-brood chicks. Interestingly, sexual dimorphism in body mass at days?8–9 post-hatching markedly differed between broods, first-brood males being 4.7% and second-brood males 22.7% heavier than their sisters, respectively. Pre-fledging mortality occurred among second-brood chicks only and was strongly female-biased. Our findings suggest that starling chicks, even if in poor conditions, are little affected by a bacterial challenge, at least in the short-term. Moreover, our study indicates that sex differences in body size, possibly mediated by sex-specific maternal investment in egg size, may heavily impact on pre-fledging survival in a different way in the course of the breeding season, resulting in sex-specific seasonal decline of offspring fitness. Finally, we suggest that levels of circulating antioxidants should be regarded among the proximate causes of the association between timing of fledging and long-term survival in avian species.     

Non-adaptive adoptions of nestlings in the colonial lesser kestrel: proximate causes and fitness consequences

We examined the causes, costs and benefits of adoption in the altricial lesser kestrel Falco naumanni. Specifically, we tested the intergenerational conflict hypothesis, proposed to explain adoption in some birds. Adoptions involved 76% of the nests and 51% of the nestlings at a mean age of 25 days (12 days before fledging). Nest-switching nestlings were not in poorer body condition, more parasitized or younger than their siblings, and body condition and prey delivery rates of their parents did not differ from those of other parents. In the foster nest, adopted nestlings did not benefit from higher feeding rates or a prolongation of the nestling period. They did not have fewer nest-mates or achieve higher rank within the new brood. Thus, adopted nestlings did not improve their body condition and survival. Adult lesser kestrels seemed unable to finely discriminate beween their own and alien chicks. Foster parents bore the cost of an increase of prey delivery rates, although it did not affect their survival or subsequent reproductive performance. Therefore, our results do not support the intergenerational conflict hypothesis, and suggest that adoption in this species is non-adaptive. Traditionally, the lesser kestrel bred in cliffs where movement among nest-sites was restricted. Nowadays, about half of the colonies are in tiled roofs which facilitate nest-switching by nestlings. The high rate of adoptions may thus be explained as reproductive errors associated with the recent occupation of a new breeding habitat. Received: 3 May 1996 / Accepted after revision: 19 January 1997     

Cooperative breeding by the Galápagos mockingbird,Nesomimus parvulus

Summary The costs and benefits of helping behavior were analyzed for 36 pairs of the Galápagos mockingbird, Nesomimus parvulus, and their associates. Helping at the nest is usually done by sons or males suspected to be offspring of the breeders. Costs and benefits to breeders were assessed by comparison of pairs with and without helpers, and costs and benefits to helpers were assessed by comparison of birds which help and those which establish themselves as novice breeders.Helping behavior benefits breeders by increasing fledging success and by reducing the adult energy load in territory defense and feeding of nestlings. Breeders assisted by helpers may also benefit by decreased nest predation. Helpers enhance their inclusive fitness by helping, and gain directly by increasing their chances of securing a territory. Helpers do not appear to gain any fitness advantage from the experience of assisting, nor do they increase their survivorship by remaining on natal territory.Ecological and demographic features such as saturated territories and low territory turn-over rates due to high adult survival may be primarily responsible for the evolution of the helping behavior, with kinselection reinforcing it. Associated features of this system are a male-biased population sex ratio, a greater energetic benefit to breeding males than to breeding females in having helpers, earlier dispersal and breeding by females than by males, and much more frequent helping by males than by females. These are interpreted as consequences of brothersister aggression that indirectly minimizes the chances of inbreeding.     

Older can be better: physiological costs of paternal investment in the Florida scrub-jay

In species that undergo actuarial senescence, the value of current reproduction is predicted to increase relative to the value of future reproduction with age, as the probability of survival to another reproductive event is reduced. Therefore, life history theory predicts that aging animals should increase their investment in reproduction. However, an increase in reproductive investment may carry significant costs to the breeding individuals. We recorded provisioning rates of Florida scrub-jay male breeders, followed by their immediate capture to assess body condition and collect blood for an in vitro test of immunocompetence and an assay of baseline corticosterone for a measure of stress. Older males provisioned offspring and brooding mates at the highest rates. There was no evidence of any physiological deficits in males with high provisioning rates, independent of age. It appears that birds that survive to old age are high quality birds that maintain good physiological condition, which complements the value of experience and permits maximal investment in offspring.     

Impact of helpers on colony productivity in a primitively eusocial bee

Small societies of totipotent individuals are good systems in which to study the costs and benefits of group living that are central to the origin and maintenance of eusociality. For instance, in eusocial halictid bees, some females remain in their natal nest to help rear the next brood. Why do helpers stay in the nest? Do they really help, and if yes, is their contribution large enough to voluntarily forfeit direct reproduction? Here, we estimate the impact of helpers on colony survival and productivity in the sweat bee Halictus scabiosae. The number of helpers was positively associated with colony survival and productivity. Colonies from which we experimentally removed one helper produced significantly fewer offspring. However, the effect of helper removal was very small, on average. From the removal experiment, we estimated that one helper increased colony productivity by 0.72 additional offspring in colonies with one to three helpers, while the increase was smaller and not statistically significant in larger colonies. We conclude that helpers do actually help in this primitively eusocial bee, particularly in small colonies. However, the resulting increase in colony productivity is low, which suggests that helpers may be constrained in their role or may attempt to reproduce.     

The effects of helpers in cooperatively breeding purple gallinules

Summary The effects of helpers in a population of cooperatively breeding purple gallinules (Porphyrula martinica) were examined. All young birds past the age of 2 months helped feed and protect subsequent broods of chicks and participated in territorial defense. Most helpers remained on their natal territories for approximately 1 year. The number of helpers varied both among and within breeding groups. Clutch production and chick survival were related positively to the number of helpers in the group. The increase in chick survival was independent of several measures of territory quality. Helpers possibly aided chick survival by provicing extra food for the chicks and decreasing predation risk. Helpers were necessary in order for a breeding pair to keep a territory long enough to produce more than one clutch of eggs. A change in the number of helpers (increase or decrease) often was followed by a similar change in territory size. These results suggest that purple gallnule helpers can increase the reproductive success of the breeding group and may be vital for the continued maintenance of a breeding territory.     

Influence of kinship on helping behavior in Galápagos mockingbirds

Summary The social organization of the Galápagos mockingbird (Nesomimus parvulus) in unusual in that groups frequently include more than one breeding pair (plural breeding), and helping behavior is flexible: some birds neither breed nor help, while others do both. To investigate the influence of kinship on helping behavior, I categorized each bird as a helper or non-helper with respect to each nest within its group where it had an opportunity to help. The incidence of helping varied with relatedness: more birds helped when nestlings available to be fed were close relatives than when not. This result was independent of a higher incidence of helping among males than among females and of variation with age among males. Proportionally more nonbreeding than breeding males helped, but breeding and nonbreeding females helped equally infrequently; breeders helped most often after their own nests failed. The incidence of helping was highest among birds with opportunities to feed offspring of breeders that had fed the potential helper as a nestling, suggesting a mechanism for kin discrimination based on associative learning. Juveniles with opportunities to choose among alternative recipients preferentially fed closely related nestlings, but insufficient information was available to determine if adults also did so. Kinship did not influence the rate at which nestlings were fed by helpers. Juveniles fed nestlings at lower rates than did adult helpers, but helping effort was otherwise unaffected by age, sex, or relatedness. Limitation of help to former feeders functions as a mechanism for directing aid to relatives in a plural breeding system where degrees of kinship vary among potential recipients within the same group.     

Cooperative breeding and immunity: a comparative study of PHA response in African birds

Cooperatively breeding birds might be expected to suffer from higher costs of parasitism than pair-breeding species because of two aspects of their ecology which should facilitate horizontal transmission and possibly select for higher parasite virulence: first, they interact regularly with more individuals than pair-breeding species, and second, these individuals are commonly close relatives that could share similar resistance alleles. This hypothesis predicts that cooperative breeders should invest relatively more in immune defence than closely related species which breed in pairs. I tested this prediction comparatively in African birds by examining the response of the immune system to the mitogenic lectin, phytoahemagglutinin (PHA response) in relation to cooperative breeding. Among 66 species, of which 18 breed cooperatively, PHA response was significantly higher in cooperatively breeding species. This association appeared not to be confounded by body size, clutch size, nest position, coloniality or similarity owing to common phylogenetic descent. These results suggest that cooperatively breeding birds may have been selected to invest more than pair-breeders in defences against parasites. If so, then additional costs of philopatry and helping behaviour might be imposed on breeders, helpers and offspring.     

Vitamin E supplementation enhances growth and condition of nestling barn swallows (Hirundo rustica)

To optimize fitness, organisms may have to trade the number and quality of individual offspring against their own condition and survival. Limiting micronutrients such as antioxidants may be crucial to this trade-off. We investigated whether vitamin E, a major antioxidant in the diet of vertebrates, is limiting to barn swallow (Hirundo rustica) nestlings. We manipulated brood size to alter the intensity of sib–sib competition and supplemented nestlings with two different physiological doses of vitamin E while establishing a control group. Treatment effects were measured on body mass and size, feather growth, T cell-mediated immune response and hematocrit. Supplementation with vitamin E at intermediate physiological doses improved nestling mass and condition and feather growth, whereas higher physiological doses did not enhance offspring quality compared to a control treatment. The positive effects of vitamin E on body mass and condition were only detectable from days 6 to 10 when maximum growth rate is attained. Experimental enlargement of broods reduced body mass and size and T cell-mediated immune response only during the late nestling period. The effect of vitamin E supplementation did not depend on brood size manipulation, as revealed by the nonsignificant statistical interaction. This result contradicts the hypothesis that availability of vitamin E depends on intrabrood competition and instead suggests that it depends on concentration of vitamin E in the insect prey of swallows. Thus, antioxidants may be available in limited amounts to barn swallow nestlings and such limitation affects growth. In addition, present results confirm that barn swallow parents trade progeny number against growth and immunity of individual offspring.     

Cooperative breeding in purple gallinules: the role of helpers in feeding chicks

Summary The participation of breeders and helpers in the feeding of 21 broods of chicks was studied in a population of cooperatively breeding purple gallinules (Porphyrula martinica). In the breeding group, all birds over the age of 2 months fed chicks. Female breeders fed chicks at the highest rate, followed by male breeders and adult helpers, old juvenile helpers, and young juvenile helpers. The amount of food breeders fed chicks was independent of the number of helpers in the breeding group. However, breeders made fewer feeding visits when they had helpers. Male and female breeders spent similar amounts of time feeding chicks. Helpers spent significantly less time feeding chicks than did breeders. As helpers grew older they fed chicks at a faster rate, made more feeding visits and spent more time feeding chicks. Analysis of variance was used to determine which variables explained the variation in the brood feeding rate (amount of food delivered to an entire brood during one observation). Age of chicks had a significant nonlinear effect, and size of brood and number of helpers had significant linear effects on the brood feeding rate. Chicks in groups with helpers received more food and were accompanied for longer periods of time than chicks in groups without helpers; either or both of these factors may have led to increased chick survival.     

Food allocation rules vary with age and experience in a cooperatively breeding parrot

Although it is known that parents can differ in their optimal resource allocation to offspring in size-structured broods, the mechanisms determining differences in allocation rules of carers are not yet clarified. In cooperatively breeding species, breeders and non-reproductive helpers often differ in their fitness payoffs of providing care and in their breeding experience. Cooperative breeders thus provide an appropriate system to examine two hypotheses originally proposed to explain differences in food allocation among parents: (i) food allocation between carers differs because of the distinct cost-benefit ratio of selective feeding (i.e. breeders and helpers are expected to differ in food allocation) and (ii) carers differ in their ability to feed selectively (i.e. differences in food allocation are expected between experienced adults and inexperienced yearlings). We compared feeding rates with which breeders, old helpers and yearling helpers provisioned nestlings of different hatching rank. The influence of experience upon food allocation was further assessed by comparing food allocation of yearlings early and late during nesting. We show that allocation rules differ between age classes because breeders and old helpers fed the youngest chicks most, whereas yearlings showed the opposite pattern. The role of experience was supported by the fact that yearlings adjusted food allocation to that observed in experienced adults during the breeding season. We thus suggest that food allocation in El Oro parakeets depends either on differential skills of adults to transfer food to the youngest chick or on their ability to recognize nestling needs.     

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.     

Do helpers increase reproductive success?

Summary Although several different hypotheses have been proposed to explain the evolution of helping behavior, most are based on the assumption that helping enhances the reproductive success of recipient breeders. I tested this assumption by removal experiments in the cooperatively breeding Florida scrub jay (Aphelocoma c. coerulescens). This species lives in permanently territorial social units containing a single breeding pair and none to six nonbreeders, which are usually offspring of the breeding pair and which usually act as helpers by feeding the nestlings and fledglings produced by the breeding pair. Although experimental removals of non-breeders in 1987–1988 had no significant effect on breeder survival, egg production, or hatching success, experimental groups suffered higher rates of predation on nestlings (1987) and lower rates of fledgling survival (both years) than did unmanipulated controls. As a result, experimental groups produced an average of only 0.56 independent juveniles, compared to 1.62 young for controls. Analysis of the factors contributing to nestling and fledgling mortality indicates that helping behavior per se (i.e., the aid that nonbreeders provide to dependent young), not the mere presence of nonbreeders, was responsible for the greater reproductive success observed in control groups. Because survival rates of allofeeders (i.e., those nonbreeders that provisioned dependent young) were virtually identical to those of non-allofeeders, the costs of helping behavior in this species appear to be small. Furthermore, nonbreeders are more likely to provision dependent young within their social unit when those young are closely related. I therefore conclude that nonbreeders increase their indirect fitness by serving as helpers and that helping behavior in the Florida scrub jay is a trait that has current selective utility. It remains debatable, however, whether helping in this species is an adaptation that has been shaped by the process of natural selection.     

Carer provisioning rules in an obligate cooperative breeder: prey type, size and delivery rate

Providing food to developing offspring is beneficial for offspring but costly for carers. Understanding patterns of provisioning thus yields important insights into how selection shapes (allo-) parental care strategies. Broadly, offspring development will be influenced by three components of provisioning (prey type, size and delivery rate). However, all three variables are rarely considered simultaneously, leading to suggestions that the results of many studies are misleading. Additionally, few studies have examined the provisioning strategies of breeders and non-breeding helpers in obligate cooperative breeders, wherein reproduction without help is typically unsuccessful. We investigated these components of provisioning in obligately cooperative chestnut-crowned babblers (Pomatostomus ruficeps). Prey type was associated with size, and delivery rate was the best predictor of the overall amount of food provided by carers. As broods aged, breeders and helpers similarly modified the relative proportion of different prey provided and increased both prey size and delivery rate. Breeding females contributed less prey than male breeders and adult helpers, and were the only carers to load-lighten by reducing their provisioning rates in the presence of additional carers. While our results suggest that breeders and helpers follow broadly comparable provisioning rules, they are also consistent with the idea that, in obligately cooperative species, breeding females benefit more from conserving resources for future reproduction than do helpers which have a low probability of breeding independently.     

Flexible helper structure as an ecological adaptation in the pied kingfisher (Ceryle rudis rudis L.)

Summary The pied kingfisher has two types of helpers at the nest: primary ones, helping their own parents, and secondary ones, helping birds other than parents. Primary helpers are always accepted by breeding pairs, secondary helpers only in poor environmental conditions where the time and energy budget of parents is not sufficient for rearing the offspring alone. Under these conditions, helpers increase the breeding success of pairs (Tables 2 and 3) by providing additional food for the young (Table 4). Thus the flexible helper structure can be seen as an ecological adaptation. It is argued that-originating from a skewed sex ratio and breeding in colonies-this adaptation evolved through the combined effects of individual and kin selection.     

Helpers in colonial cooperatively breeding sociable weavers <Emphasis Type="Italic">Philetairus socius</Emphasis> contribute to buffer the effects of adverse breeding conditions

Some studies on the effects of helpers in cooperatively breeding vertebrates show a positive effect of helper presence on reproductive output whereas others find no effect. One possibility for this discrepancy is that helpers may have a positive effect when breeding conditions are adverse, while their effect might go unnoticed under good conditions. We investigate this hypothesis on sociable weavers Philetairus socius, a colonial cooperatively breeding passerine that inhabits a semi-arid region where breeding conditions vary markedly. We used multivariate mixed models to analyse the effect of helpers on reproduction under contrasting environmental and social conditions while controlling for parental and colony identity. We found that reproductive success in sociable weavers was primarily influenced by nest predation and rainfall. In addition, colony size was negatively associated with hatching and fledging success and number of young fledged per season. Helpers had a less prominent but significant influence on feeding rates and reproductive outcome. In agreement with expectations, the presence of helpers counteracted some of the negative effects of breeding in periods of low rainfall or in large colonies and was also associated with an increased number of young fledged per season. Our results illustrate that the effect of helpers might be detectable mostly under unfavourable conditions, but can contribute to improve reproductive performance in those situations.     

A critical analysis of ‘false-feeding’ behavior in a cooperatively breeding bird: disturbance effects,satiated nestlings or deception?

‘False feeding,’ where helpers arrive at nests with food but fail to provision the young, has been reported in several cooperative species. This and other potentially ‘deceptive’ behavior has been interpreted as indicating that helping may operate as a signal within such social groups. We critically examine these phenomena in the provisioning behavior of the bell miner Manorina melanophrys. Excessively close observation distances can artificially elevate the rate of false feeding in this (and other) species, but once this had been accounted for, there was little evidence for any ‘deceptive’ behavior by helpers or breeders. Natural and experimentally induced variation in the presence of a potential conspecific audience at the nest did not have any consistent influence upon the rate of false feeds, which was low at 7.94% of 6,880 nest visits. Instead, encountering unexpectedly low levels of brood demand provided a more parsimonious explanation for those visits where helpers failed to feed nestlings or ate the food themselves. Failure to completely transfer a load to nestlings was more likely when the load contained a high proportion of sticky lerp, indicating a simple prey-transfer problem. Finally, individuals that arrived at nests without prey were often members of neighboring breeding pairs, suggesting that these few non-feeding visits may instead involve an information-gathering function. We, therefore, suggest that future studies explicitly exclude the possibility of observer disturbance and all aspects of normal provisioning behavior before applying the terms ‘false feeding’ or ‘deceptive’ and inferring anything more than straightforward helping at the nest.     

Nest defence by song sparrows: methodological and life history considerations

Summary Several aspects of nest defence behavior were investigated in song sparrows (Melospiza melodia) in eastern Ontario. Two independent tests were made of the hypothesis that the increase in nest defence observed through a nesting attempt is due to the birds becoming familiar with the nest threat, rather than because the nest contents increase in value to the parents. Neither test supported the hypothesis. As predicted by life history theory for species with age-independent mortality, males did not defend their nest more vigorously as they become older. Parents defended their nests less vigorously through the breeding season, contrary to the expected pattern of increased nest defence in response to declining renesting potential. This result may be attributable to a decline in offspring value through the breeding season. Nest defence behavior of mated individuals was positively correlated, independent of factors such as offspring age, renesting potential and brood size. From this result it is proposed that a source of variation in nest defence behavior may be individuals basing their own response on their mate's response in a positive feedback fashion. Males defended nests less vigorously than females, consistent with the expectation that males have lower certainty of parentage in the offspring. It is proposed that variation in paternal uncertainty could contribute to the unexplained variation reported in nest defence studies.     

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     

Intra-group relatedness affects parental and helper investment rules in offspring care

In any system where multiple individuals jointly contribute to rearing offspring, conflict is expected to arise over the relative contributions of each carer. Existing theoretical work on the conflict over care has: (a) rarely considered the influence of tactical investment during offspring production on later contributions to offspring rearing; (b) concentrated mainly on biparental care, rather than cooperatively caring groups comprising both parents and helpers; and (c) typically ignored relatedness between carers as a potential influence on investment behavior. We use a game-theoretical approach to explore the effects of female production tactics and differing group relatedness structures on the expected rearing investment contributed by breeding females, breeding males, and helpers in cooperative groups. Our results suggest that the breeding female should pay higher costs overall when helpful helpers are present, as she produces additional offspring to take advantage of the available care. We find that helpers related to offspring through the breeding female rather than the breeding male should contribute less to care, and decrease their contribution as group size increases, because the female refrains from producing additional offspring to exploit them. Finally, within-group variation in helper relatedness also affects individual helper investment rules by inflating the differences between the contributions to care of dissimilar helpers. Our findings underline the importance of considering maternal investment decisions during offspring production to understand investment across the entire breeding attempt, and provide empirically testable predictions concerning the interplay between maternal, paternal and helper investment and how these are modified by different relatedness structures.