The role of helpers in feeding chicks in cooperatively breeding green (red-billed) woodhoopoes

Summary Observations were made of ten green (red-billed) woodhoopoe Phoeniculus purpureus flocks during the breeding season in order to quantify the relationship between flock size and the amount of food delivered to chicks. The study period was kept short specifically to minimize the effects of environmental stochasticity. Neither woodhoopoe feeding visit rates nor the total amount of food brought to chicks increased with flock size. Although nonbreeders did not increase the net rate of food provisioning to chicks, they reduced parental input in chick rearing, and hence energy expenditure by the breeding pair. However, over an 8-year study period, which includes data for 144 flock years, this did not result in increased breeding frequency or enhanced survival of breeders. There is thus no evidence that helpers' feeding contributions to young per se influence the indirect fitness of helpers.     

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.     

Seasonal variation in male-female competition,cooperation and selfish hoarding in a monogamous songbird

Both cooperation and conflict between the sexes are commonplace in monogamous mating systems. However, little is known about how cooperation and competition varies seasonally in monogamous species that maintain permanent territories. We presented territorial pairs of male and female New Zealand robins (Petroica australis) with a large supply of insect prey at monthly intervals for 2 years. Behavioural observations after food presentation were then made to quantify seasonal and sexual differences in aggressive interactions over prey, prey acquisition rates, mate provisioning, offspring provisioning, selfish food hoarding and cache retrieval. Data were used to evaluate sex-specific behavioural strategies of mediating competition for food. Results showed that males aggressively excluded females from experimental food sources year-round. Females only accessed food sources when males left them unattended. Consequently, females acquired fewer prey than males. After controlling for differences in prey acquisition, both sexes consumed similar amounts of prey in the non-breeding season. Even though males aggressively excluded females from accessing food sources directly, males fed large amounts of prey to females during the breeding season. Both sexes provisioned young at similar rates. Males cached less prey than females in the breeding season but more prey than females in the non-breeding season. Females showed similar caching intensities year-round. Although males tried to defend their hoards, females frequently retrieved male-made caches. Overall, results showed that although New Zealand robins cooperate to raise offspring during the breeding season, conflict between the sexes occurs year-round. Males and females display different behavioural strategies to gain access to experimental food sources, which appear to lessen male–female competition for food and evenly distribute food resources between the sexes.     

Do stress hormones suppress helper reproduction in the cooperatively breeding red-cockaded woodpecker (<Emphasis Type="Italic">Picoides borealis</Emphasis>)?

In the cooperatively breeding red-cockaded woodpecker (Picoides borealis), male helpers are subordinate to male breeders and do not mate with females, even when unrelated to the breeding female within their group or through extra-group matings, yet exhibit reproductive hormone profiles similar to those of breeders. We investigated whether reproduction might be suppressed in helper males via high levels of the stress hormone corticosterone. We also examined effects of group size and season on corticosterone levels by comparing baseline and maximal plasma levels of corticosterone between helper males and breeding males, and among helper males and breeders of both sexes living in groups of different sizes throughout the reproductive cycle. We also measured plasma levels of estrogen, progesterone, and testosterone to examine other potential hormonal differences between helpers and breeders. Male status did not explain variation in any hormones; therefore, our data do not support the hypothesis that helper males are reproductively suppressed via corticosterone or the other hormones investigated. However, the presence of two or more helper males in a group tended to reduce baseline corticosterone in breeding and helper males, but not breeding females, suggesting that helper males reduce parental effort of other male group members. Seasonally, maximal corticosterone peaked during the nestling provisioning phase for breeding and helper males, but not breeder females, suggesting that males show an increased response to stressors posing a potential threat to survival of offspring.     

Social system and reproduction of helpers in a cooperatively breeding cichlid fish (Julidochromis ornatus) in Lake Tanganyika: field observations and parentage analyses

It is suggested that some fish of the genus Julidochromis, substrate-brooding Tanganyikan cichlids with biparental care, breed cooperatively with helpers. We studied the social system of J. ornatus in the wild and analysed genetic parentage using microsatellites. Within the studied population three patterns of social system were identified: monogamous pairs (61%, 44 of 72 groups), pairs with helpers (29%, 21), and polygamous harems with helpers (controlled by either a large female or large male owner; 10%, 7). In cooperatively breeding groups, the number of helpers at each nest ranged from 1 to 6 (median 1), and male helpers were more numerous than female helpers. In both sexes, the body size was different among individuals of different social status (harem owner > breeder > helper). Helpers and harem owners of both sexes exhibited brood defence although its frequency was low. The molecular analysis revealed that (1) the helpers were mostly unrelated to dominant breeders, (2) many helpers of both sexes contributed genetically to the next generations, (3) male helpers had high siring success (41% of young in total), and (4) large young unrelated to group members were detected at 30% of observed nests, which may be due to breeder (or helper) replacements and immigration of young. We discuss the implications of these results for understanding the complex social system of this species, especially the low reproductive skew in comparison with other cooperatively breeding cichlids.     

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.     

Variation in male courtship costs in butterflies

A cost of mating is common to both sexes but has predominantly been examined in females. In species where males provide resources to females at copulation, male mating costs are expected to be high as nutrient provisioning enhancing female fecundity is assumed to carry costs. In addition, males frequently court females prior to mating, which is known to carry survival costs to both sexes. However, the magnitude and basis of variation in males’ mating costs remains largely unknown. Here, I examine the effect of nutrient provisioning and courtship on male longevity across full-sib families in the paternally investing green-veined white butterfly, Pieris napi. Copulating males suffered a survival cost as did courting males prevented from copulating, indicating the courtship component of mating is costly. Male P. napi release aphrodisiacs during courtship to promote mating, indicating that these compounds may also be costly to produce. Contrary to expectation, nutrient provisioning was not associated with reduced survival relative to males only allowed to court females, although it is possible that this could be masked by the potentially elevated courtship rates of courting males relative to mating males. Families differed in magnitude of reduced male survivorship, indicating a likely genetic basis to variation in costs of courtship and copulation. Male weight was unrelated to longevity and mating success, whereas longevity strongly influenced male mating success, indicating lifespan is an important male fitness trait in this species.     

Plasma levels of androgens and gonadal development of breeders and helpers in the bell miner (Manorina melanophrys)

Plasma concentration of androgens and gonad development were studied in wild cooperatively breeding bell miners (Manorina melanophrys) of different age, sex and social status. Plasma levels of androgens increased with age of birds. For sexually mature (SM) bell miners, androgen levels were higher in breeders than in nonbreeding (NB) helpers (P < 0.005), and they were marginally higher in females than in males (P < 0.10). Thus female breeders showed the highest plasma levels of androgens. This pattern may be explained by an asymmetry between the sexes in the levels of competition needed to reach and defend breeding status; the degree of intra-sexual competition seems to be higher among female bell miners than among males. In general, male breeders had larger gonads than male SMNB helpers; male breeder gonads produced spermatozoa whereas most helpers' gonads did not. However, old (i.e. 34 months) SMNB male helpers had large gonads producing spermatozoa in spite of having low plasma levels of androgens. We suggest that young male bell miners may be under a voluntary mechanism of reproductive suppression perhaps favoured by inbreeding avoidance; although some aggressive interactions observed between very young helpers (about 2 months) and adult members of the breeding unit suggests that a certain degree of imposition also occurs at young ages. Older male helpers may avoid aggression with the male breeder and imposed reproductive suppression, hence the low circulating levels of androgens, but they have the potential to sneak extra-pair copulations. Gonad size decreased during the non-breeding season in both sexes.     

Compensating for the costs of polygyny in hen harriers Circus cyaneus

In polygynous species, the adults are faced with a dilemma during chick rearing. Males must decide how to distribute food between their females and food allocation patterns are often highly unequal. In turn, the females that receive less food from males have to decide how much time to invest in additional hunting. If they spend more time hunting, then they leave their young exposed to weather and predators. However, if they stay at the nest, they increase the risk of their chicks starving. One way that birds may compensate for reduced provisioning is by increasing the size of prey caught. We tested this hypothesis by comparing prey deliveries to nests of hen harriers, Circus cyaneus, with females of different breeding status. As expected, male harriers delivered less food items to the nests of polygynous females, and especially their secondary, or β females. However, both sexes were able to compensate by delivering larger items and there was no difference in the overall mass of food delivered to nests. Moreover, females spent a similar amount of time at the nest, irrespective of status, and there were no overall differences in breeding success. Our results show that polygynous female harriers can compensate for the costs of polygyny, but we suggest that their ability to do so will vary according to the abundance of both large prey and predators.     

Siblicide in the cooperatively breeding laughing kookaburra (Dacelo novaeguineae)

I describe siblicide in the laughing kookaburra (Dacelo novaeguineae), a reverse size-dimorphic, cooperatively breeding kingfisher. Clutches were usually of three eggs, and nestlings hatched asynchronously, with intervals of 2–72 h between successive eggs. Siblicide occurred in two temporally and mechanistically distinct episodes. The youngest nestling died in one-third of all nests within days of hatching as a result of aggression from its elders. Kookaburra nestlings attacked each other using a hook on their upper beak – a rare example of a morphological specialisation for sibling rivalry. In one-fifth of all nests, the youngest nestling starved to death much later, without overt aggression, when nestling growth rates were highest. I examined the effects of food availability and competitive disparities between nestlings on the incidence of both types of siblicide. The probability of late, starvation-mediated mortality was negatively correlated with the number of male helpers. Early, aggressively mediated siblicide occurred in nests characterised by a suite of correlated variables that I call the ”kookaburra siblicide syndrome”: (1) no male helpers attended the nest, (2) the third-hatched nestling was much smaller than the second-hatched nestling, (3) the first and second nestling to hatch were male and female, respectively, and (4) there was a short hatch interval between the first two nestlings. The kookaburra siblicide syndrome variables could be inter-correlated if they were all related to the female’s condition at the onset of incubation. Females in poorer condition may be less likely to have male helpers, more likely to lay small third eggs, and more likely to hatch the first two eggs relatively synchronously because of nutritional constraints during the onset of incubation. These females may further promote siblicide by modifying the sexes of the first two nestlings. If a female hatches soon after an older but eventually smaller brother, dominance between the first two nestlings could be destabilised. I suggest this leads to escalated aggression in the nest and the death of the third nestling, which is least able to defend itself. Received: 17 December 1999 / Received in revised form: 8 May 2000 / Accepted: 20 May 2000     

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.     

Helpers-at-the-nest have the same provisioning rule as parents: experimental evidence from play-backs of chick begging

Despite the success of kin selection in explaining helping-at-the-nest among communally breeding birds, we know almost nothing about how helpers regulate their chick-feeding effort. This is especially interesting given how much we now know about parental provisioning `rules-of-thumb' and the evolution of chick begging as an honest signal of `need'. This study explores the provisioning rules of helpers and parents in Arabian babblers (Turdoides squamiceps), using tape play-backs to supplement chick-begging signals and increase apparent brood demand. In all eight groups tested, both helpers and parents fed older, noisier broods at higher rates. Total provisioning rates to nests increased during begging play-back days compared to control days. Absolute provisioning rates by helpers and the scale of their responses to play-backs were statistically indistinguishable from those of parents. In both helpers and parents, increases in nest visits during play-backs were associated with reductions in foraging distance from the nest and increases in size of prey delivered. Older birds of both sexes delivered slightly larger prey items, possibly reflecting differences in foraging ability due to experience. These results are consistent with the idea that, like the parents, helpers-at-the-nest in Arabian babblers provision nestlings as part of a strategy of investment, irrespective of helper age, dominance status or sex. In this species, high relatedness within groups may provide parents and helpers with similar kin-selected fitness benefits, although the mutualistic advantages to helpers from simply augmenting group sizes cannot be ruled out. Received: 17 June 1997 / Accepted after revision: 28 February 1998     

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.     

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.     

Female nutritional state affects the rate of male incubation feeding in the pied flycatcher Ficedula hypoleuca

Summary Male pied flycatches Ficedula hypoleuca regularly feed their mates during incubation. By experimentally supplying some females with extra food we studied how the female's nutritional state affected her incubation schedule and the rate at which her mate fed her. Females that received extra food spent more time on the nest and shorter periods away from it, compared with control females. This suggests that nest attentiveness is governed by the amount of energy available to the female. When females reccived extra food, males decreased their rate of incubation feeding. They also did so in response to increasing ambient temperatures, whereas incubation schedules were unaffected. We, therefore, conclude that our results support the female nutrition hypothesis, i.e., that the food provided by the male constitutes a significant nutritional contribution to the incubating female.     

Experimental evidence for food limitation and sex-specific strategies of American kestrels (<Emphasis Type="Italic">Falco sparverius</Emphasis>) provisioning offspring

For birds with altricial young, the brood-rearing period is one of the most energetically expensive periods in their lives and may be the bottleneck for fitness. Because parents are expected to be prudent in allocating resources between reproduction and self-maintenance, food supply should be an important factor determining reproductive decisions during brood rearing. Parents with abundant food are expected to have enhanced fitness because they are able to reduce their work rates and increase their own survival chances, because their offspring may be of higher quality, or some combination of these. However, few studies have simultaneously documented all of these variables in a single investigation. We performed a food supplementation experiment to test how food supply influenced provisioning decisions by parent American kestrels (Falco sparverius). Female kestrels showed a strong response to extra food and reduced their provisioning rates. As a result, supplemented females had higher return rates than control females, suggesting significant effects of food on female survival. Because females used extra food to increase their fitness, our results suggest that kestrels raising offspring are limited by food. Male kestrels whose nests were supplemented also responded to extra food by reducing provisioning, but to a much lesser extent than their mates. Male parents did not appear to benefit from supplementation, as their return rates were similar to control males. The total amount of food received on a daily basis by nestlings was similar between supplemented and control nests. Supplemented offspring therefore did not fledge in better condition or have higher survival rates than control nestlings; the only significant factor consistently affecting offspring condition and survival was weather.     

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.     

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.     

Food supply during prelaying period modifies the sex-dependent investment in eggs of Eurasian kestrels

The theory of sex allocation suggests that if the reproductive value and the cost of producing/rearing offspring differ between male and female offspring, parents should invest differently in sexes depending on environmental conditions. Female parents could allocate more resources to eggs of one sex to compensate potential sex-dependent constraints later during the nestling period. In this study, we tested the influence of environmental conditions on sexual dimorphism in eggs of Eurasian kestrels (Falco tinnunculus) by experimentally manipulating food availability before laying. We found that an increase in food abundance before laying did not increase egg mass but changed sex-dependent resource distribution in eggs. In food-supplemented pairs, but not in control pairs, egg mass and hatchling mass were similar between males and females. In addition, we found, in the food-supplemented group, that the latest hatched females showed shorter hatching times than in the control group. In control pairs, female eggs, hatchlings and nestlings were heavier than males. In addition, male fledglings in the food-supplemented group gained less mass than those in the control group. As that food abundance was only increased until the onset of laying, female kestrels were expected to invest in eggs taking food abundance before egg formation as a predictor of future conditions during brood rearing. Our study shows that environmental conditions before laying promote a subtle adjustment of the resources invested in both sexes of offspring rather than in other breeding parameters. This adjustment resulted in a shortening of hatching time of the last hatched females that possibly gives them advantages in their competitive capacity with respect to male nest-mates.     

Male characteristics,parental quality and the study of mate choice in the red-winged blackbird (Agelaius phoeniceus)

Summary A demonstration of adaptive mate choice by females in resource-defence mating systems requires clear predictions as to how females should rank breeding situations (defined by the quality of both the resident male and the territory he defends) so as to maximize their fitness. Since male quality is only weakly correlated with territory quality in red-winged blackbirds (Agelaius phoeniceus), ranking breeding situations in this species will require a consideration of both those parameters independently of each other as long as both vary among males, are predictable before mating, and affect female fitness. Data from a two year study of an eastern Ontario population of this species suggested that two components of male parental quality, nest defence effort and provisioning of nestlings with food, both varied among males and were somewhat predictable. Two measures of nest defence effort were correlated with an index of epaulet size (a reliable predictor of captive dominance rank in this species) (Table 5), and provisioning appeared to be predictable on the basis of both courtship behavior and breeding experience. Our data also suggest that these two components of male parental quality do not covary. Since male provisioning tends to be restricted to the nestlings of the primary and secondary mates in this species, breeding situations must be ranked not only with respect to their manifold quality but also with respect to the mating status of individual females.