Parent blue-footed boobies suppress siblicidal behavior of offspring

Behaviorally dominant nestlings routinely kill sibling nestmates in blue-footed booby (Sula nebouxii) broods during periods of food shortage. Previous work demonstrated that these dominant, first-hatching “A-chicks” regulate the lethality of their behavior towards subordinate, second-hatching “B-chicks,” showing tolerance towards B-chicks except during chronic food shortages. Siblicide by A-chicks usually occurs after the hatchling stage. Results of an interspecific cross-fostering experiment indicated that A-chicks also attempt siblicide shortly after hatching, but parents apparently exert control over these attempts, and thwart them, when chicks are young. Theory predicts selection for such regulation in siblicidal birds that are likely to experience genetic parent-offspring conflict over the value of subordinant nestlings; our evidence of post-hatching parental regulation is consistent with that prediction. Received: 6 June 1998 / Accepted after revision: 12 July 1998     

Sibling aggression, hatching asynchrony, and nestling mortality in the black kite (Milvus migrans)

In siblicidal species, hatching asynchrony could act to reduce sibling rivalry or promote the death of last-hatched chicks. The pattern of hatching asynchrony was experimentally altered in the black kite Milvus migrans. Hatching asynchrony in control broods was intermediate between those of experimentally synchronised and asynchronised broods. Sibling aggression and wounds on the chicks were more commonly observed early in the nestling period and in synchronous nests. Serious injuries were observed on last-hatched chicks in asynchronous nests, as were observations of intimidated or crushed chicks. Sibling aggression was related to food abundance, but some chicks died at an early age in nests with abundant food (cainism). Cainism was more commonly found in asynchronous nests. For species with facultative siblicide, moderate hatching asynchrony could be a compromise between reducing sibling rivalry and avoiding large size differences between sibs that would result in cainism. Female black kites preferentially fed the smallest chicks and exhibited behaviours to reduce sibling aggression, contrary to observations in other siblicidal species. In a highly opportunistic forager such as the black kite, a strategy may exist to protract the life of all the chicks in the brood, waiting for unpredictable situations of food overabundance. This would induce the appearance of a parent-offspring conflict over brood reduction, reflected in the existence of a possible anticipated response by some of the chicks (cainism) and in the appearance of special behaviours by the parents to selectively feed smaller chicks or reduce sibling aggression. In this facultatively siblicidal species, cainism does not seem to be the final stage of an evolutionary trend favouring the raising of high-quality chicks, but a manifestation of a parent-offspring conflict over brood size. Received: 9 March 1998 / Accepted after revision: 8 August 1998     

No reduction in aggression after loss of a broodmate: a test of the brood size hypothesis

In some vertebrate species, parents create a large brood or litter then, in the event of unfavourable ecological conditions, apparently allow the number of offspring to be adaptively reduced through siblicide. But how is sibling aggression regulated so that deaths occur only in unfavourable conditions? One proposed mechanism is brood size-dependent aggression. Two experiments tested for this mechanism by reducing three-chick broods of blue-footed boobies either during or after the period of dominance hierarchy establishment. In neither experiment did aggression of the two eldest and highest ranking chicks decline after removal of the youngest broodmate, in comparison with controls. These results suggest that dominant booby chicks do not become less aggressive to each other after disappearance of their youngest broodmate and that this species does not show brood size dependent aggression. Elder blue-footed booby chicks increase their attacks on broodmates when they receive less food, and this mechanism may be sufficient to tailor brood size to food availability.     

Evidence of kin-selected tolerance by nestlings in a siblicidal bird

Behaviorally dominant members of blue-footed booby (Sula nebouxii) broods can effect siblicide by restricting access of subordinate siblings to parents providing food. In spite of their capacity for siblicide, dominant chicks permit subordinates to feed during short-term food shortage; in fact, the proportion of the food that the dominant takes is independent of the total amount delivered in older chicks. A model of optimal food distribution suggests that dominant chicks maximize their inclusive fitness with this pattern, rather than by satisfying their own food requirements and leaving what remains for the subordinate sibling. The indirect reproductive potential represented by a chick's sibling appears to have influenced the evolution of siblicidal brood reduction in this species.     

Testosterone increases siblicidal aggression in black-legged kittiwake chicks (Rissa tridactyla)

To compete for parental food deliveries nestling birds have evolved diverse behaviors such as begging displays and sibling aggression. Testosterone has been suggested to be an important mechanism orchestrating such competitive behaviors, but evidence is scarce and often indirect. Siblicidal species provide an interesting case in which a clear dominance hierarchy is established and the dominant chicks lethally attack siblings. We experimentally elevated testosterone in chicks of a facultatively siblicidal species, the black-legged kittiwake, Rissa tridactyla, and showed that testosterone-treated chicks were more aggressive toward their sibling than were control chicks. In such facultatively siblicidal species, chicks normally exhibit intense aggression only when threatened by starvation. Indeed, we found that chicks in relatively poorer condition were more aggressive than were chicks in better condition, even among testosterone-treated chicks, suggesting the action of an additional signal modulating aggression. Relatively larger siblings were also more aggressive than were relatively smaller siblings, confirming the importance of size advantage in determining dominance hierarchies within the brood. In addition, testosterone increased aggression toward a simulated predator, indicating that in kittiwakes testosterone can increase aggression in contexts other than siblicide. Testosterone promoted aggression-mediated dominance, which increased begging although testosterone treatment did not have a significant separate effect on begging. Therefore, testosterone production in the kittiwake and most likely other siblicidal species seems an important fitness mediator already early in life, outside the sexual context and not only manifesting itself in aggressive behavior but also in dominance-mediated effects on food solicitation displays toward parents.     

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     

Is obligate siblicidal aggression food sensitive?

In avian species whose chicks show facultative siblicide, attacks increase with food deprivation. In species that show obligate siblicide, this causal relationship is not expected, but no test has been made. When we composed artificial pairs of young brown boobies, Sula leucogaster (an obligately siblicidal species), and supplied variable amounts of food to the older nestlings in each pair, food ingestion was related to the most intense form of attack, pushes, which can cause death by expelling the broodmate from the nest. The less food an older nestling ingested, the more time it spent active and the greater its rate and absolute frequency of pushes, and the more often it expelled its nestmate. Hence, deficient food provision to older nestlings could precipitate siblicidal expulsion of broodmates. Younger nestmates were aggressive too, and the more they were pushed and expelled, the more they pecked. Aggression of senior brown-booby broodmates may be flexible and food sensitive in order to optimize the timing of siblicide or to make siblicide weakly facultative.Communicated by R. Gibson     

Hatching asynchrony and survival of insurance offspring in an obligate brood reducing species,the American white pelican

American white pelicans (Pelecanus erythrorhynchos) lay two eggs but typically rear only one young owing to siblicidal brood reduction affecting the later-hatched, or B-chick. When the A-offspring fails at an early age, the B-chick may survive as a replacement (insurance) offspring. Using a combination of nests with natural and artificially manipulated hatching asynchrony, I examined the hypothesis that hatching asynchrony in this species is adaptively tuned to permit B-chicks to survive during the time they are most likely to be needed as replacements, with brood reduction following when they become redundant. Hatching asynchrony over the natural range of 0–4 days significantly increased within-brood mass differentials and reduced B-chick lifespan. Full synchrony had a marginally negative effect on A-chick mass. Greater asynchrony did not significantly affect the number of days B-chicks survived after hatching of the A-chick, owing to a corresponding extension of time B-offspring were protected from harassment while still within the egg. This resulted in a high probability (> 0.8) of B-chicks surviving through the initial period (5–7 days) of maximum early A-chick loss. Redundant B-chicks were subject to heavy brood reduction, with both chicks likely to have survived at only one each of 94 natural and 84 manipulated (0, 2, and 4 days asynchrony) nests. Hatching asynchrony in American white pelicans, in combination with a rapid development of senior chick siblicidal competence, appears to result in a time course of brood reduction appropriate for an effective insurance reproductive strategy. Received: 2 February 1996 /Accepted after revision: 18 May 1996     

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.     

The function of hatching asynchrony in the blue-footed booby

The blue-footed booby (Sula nebouxii) commonly hatches two eggs 4 days apart; then the senior (first-hatched) chick aggressively dominates the other and sometimes kills it. Two hypotheses explaining the function of the hatching interval were tested by creating broods with synchronous hatching: the facultative brood reduction hypothesis of Lack (1954) and the sibling rivalry reduction hypothesis of Hahn (1981). The results contradicted most predictions of both hypotheses: synchronous broods formed an aggressive hierarchy similarly to asynchronous broods (controls), and subordinate chicks grew poorly (Fig. 1) and died frequently, similarly to junior chicks in control broods. However, compared with synchronous broods, asynchronous broods showed less aggression (Fig. 2), diminished food allocation to subordinate chicks (Fig. 3) and less total food consumption (30% fewer feeds at age 0–10 days). These behavioral comparisons took into account the different ages of chicks in different treatments. The results suggest that natural asynchrony makes brood reduction more efficient and decreases the costs of sibling aggression to parents, in terms of their future survival or fecundity, as proposed by Mock and Ploger (1987). Further, in exaggeratedly asynchronous broods (8-day hatch interval) junior chicks suffered more aggression (Fig. 4) and grew more slowly than junior chicks in control broods. This result supports the hypothesis of optimal hatch asynchrony of Mock and Ploger (1987).     

Preferential allocation of food by magpies Pica pica to great spotted cuckoo Clamator glandarius chicks

Adult magpies Pica pica provide parasitic great spotted cuckoo Clamator glandarius nestlings with a diet very similar to that fed to their own chicks. In both naturally and experimentally parasitized nests, great spotted cuckoo chicks were fed at a higher rate than magpie chicks in the same nest. This preferential allocation of food by magpie parents to great spotted cuckoo chicks is consistent with the supernormal stimulus hypothesis, because this result implies that cuckoo chicks provide stronger stimuli for parental care than host chicks. Great spotted cuckoo chicks receive most of the food brought to the nest by the foster parents, because they exploit a series of stimuli which jointly (or sometimes individually) operate as a supernormal stimulus. This hypothesis predicts that if any stimulus is masked, the efficiency of the cuckoo in eliciting parental care will decrease. Here, we analyze experimentally the effects of two of these stimuli, preferential feeding of large nestlings and of nestlings with conspicuous palatal papillae. Firstly, when we experimentally introduced one medium-sized (7–9 days) cuckoo chick into an unparasitized magpie nest where the largest magpie chick was 12–15 days old, the cuckoo did not receive significantly more food than the average or the largest magpie chick. Secondly, when unparasitized nests were experimentally parasitized with a cuckoo chick that had its gape painted to mimic that of magpie chicks, the parasitic cuckoo received less food than the average magpie chick.     

Desperado siblings: uncontrollably aggressive junior chicks

According to the desperado sibling hypothesis, chicks of obligately siblicidal species kill their junior broodmates as early as possible because junior broodmates face dire ecological prospects and are consequently predisposed to aggressively overthrow elder broodmates by all-out aggression. The agonistic behavior of junior chicks is virtually unknown because they die so young. We investigated the agonistic behavior of hypothetical desperados by fostering junior brown boobies (Sula leucogaster, an obligately siblicidal species) into nests of the blue-footed booby (S. nebouxii, a facultatively siblicidal species) containing an older singleton blue-foot chick. Controls were junior blue-footed boobies fostered into the same situation. Junior brown boobies were 7 times more aggressive than controls and most of them dominated their elder and larger nestmates. Four of nine brown booby juniors showed relentless aggression, delivering up to 711 pecks, bites and pushes (including "expulsion pushes") per hour, thereby overwhelming nestmates 90% heavier and permanently expelling one of them from the nest. Similarly, in natural broods of two surviving brown booby chicks, the losing chick was 13 times as aggressive as blue-foot subordinates, up to at least age 7 weeks. Contrast of the two species of booby suggests the evolution of agonistic roles within broods may be partly driven by selection on potential victims to express a level and type of aggressiveness appropriate to their status-related ecological prospects.     

Seasonal nestmate recognition in the ant Formica exsecta

Under favorable conditions, the mound-building ant Formica exsecta may form polydomous colonies and can establish large nest aggregations. The lack of worker aggression towards nonnestmate conspecifics is a typical behavioral feature in such social organization, allowing for a free flux of individuals among nests. However, this mutual worker toleration may vary over the seasons and on spatial scales. We studied spatio-temporal variation of worker–worker aggression within and among nests of a polydomous F. exsecta population. In addition, we determined inter- and intracolony genetic relatedness by microsatellite DNA genotyping and assessed its effect on nestmate recognition. We found significant differences in the frequency of worker exchange among nests between spring, summer, and autumn. Moreover, we found significant seasonal variation in the level of aggression among workers of different nests. Aggression levels significantly correlated with spatial distance between nests in spring, but neither in summer nor in autumn. Multiple regression analysis revealed a stronger effect of spatial distances rather than genetic relatedness on aggressive behavior. Because nestmate discrimination disappeared over the season, the higher aggression in spring is most plausibly explained by cue intermixing during hibernation.     

Asymmetric contests at the nest

Hatching asynchrony of nestling birds leads to weight asymmetries, which in turn affect the nestlings’ relative success when competing for feedings brought to the nest. We present a game theoretic model that predicts how weight asymmetry influences the nestlings’ energy on securing feedings, thus determining the caloric value remaining for weight gain as well as the distribution of feedings obtained. The model has a unique Evolutionary Stable Strategy (ESS) profile, in which nestlings in more asymmetric nests exhibit less aggression and hence achieve larger weight gain per feeding. The impetus for this model was data from a long-term study of Arabian babblers (Turdoides squamiceps) that showed a surprising negative correlation between the number of feedings that a nest received and the overall weight gain in the nest. This finding is, however, entirely consistent with our model—in more symmetric nests, the individuals fight more and are consequently hungrier and beg for additional food, are fed more, but still gain less weight due to the higher energetic costs of fighting. The model provides a fundamental explanation also for related findings in other species, in which chicks in asynchronous broods were found to be heavier than those from synchronous broods. In addition, it supports the sibling rivalry hypothesis by which brood asynchrony may diminish aggressive interactions among nestlings, leading to more efficient use of resources.     

Cuckoo growth performance in parasitized and unused hosts: not only host size matters

The quality and quantity of food delivered to young are among the major determinants of fitness. A parental provisioning capacity is known to increase with body size. Therefore, brood parasitism provides an opportunity to test the effects of varying provisioning abilities of different-sized hosts on parasitic chick growth and fledging success. Knowledge of growth patterns of common cuckoo, Cuculus canorus, chicks in nests of common hosts is very poor. Moreover, no study to date has focused on any currently unused hosts (i.e., suitable cuckoo host species in which parasitism is currently rare or absent). Here, I compare the growth performance of cuckoo chicks in nests of a common host (the reed warbler, Acrocephalus scirpaceus) and two unparasitized hosts (the song thrush, Turdus philomelos, and the blackbird, Turdus merula). Parasitic chicks were sole occupants of the observed nests, thus eliminating the confounding effect of competition with host chicks. Experiments revealed striking differences in parasitic chick growth in the two closely related Turdus hosts. Cuckoo chicks cross-fostered to song thrush nests grew much quicker and attained much higher mass at fledging than those in nests of their common reed warbler host. Alternatively, parasitic chicks in blackbird nests grew poorly and did not survive until fledging. I discuss these observations with respect to host selection by parasitic cuckoos.     

Brown pelican siblicide and the prey-size hypothesis

Summary We asked whether the brown pelican (Pelecanus occidentalis) practices facultative brood reduction and tested two predictions of Mock's (1985) prey-size hypothesis: (1) if chicks take food directly from the parental mouth, nestmates should compete aggressively; (2) aggression between nestmates should increase during the developmental transition from indirect feeding (parents deposit food on the substrate) to direct feeding (parents pass food from mouth to mouth). Eggs in two-egg and three-egg clutches were laid and hatched 2 days apart. Junior (second- and third-hatched) chicks, fed less than their nestmates, grew more slowly and died more frequently. Of non-hatchling victims 74% were underweight, 55% bore peck wounds and 43% were found outside the nest, implying starvation, aggression and expulsion from the nest. Aggression occurred in all observed sibships, and junior chicks were subordinate in eight of ten cases. A progressive transition from indirect to direct feeding occurred during the 30 days after hatching, but there was no evidence of an increase in pecking during the transition. In conclusion, the brown pelican practices facultative brood reduction, and chick loss is mediated by sibling aggression as predicted by the preysize hypothesis. Pecking during indirect feeds seems to contradict the prey-size hypothesis, but may serve partly to establish a relationship of dominance-subordinance.Correspondence to: H. Drummond     

Low aggression levels and unbiased sex ratios in a prey-rich environment: no evidence of siblicide in Ngorongoro spotted hyenas (<Emphasis Type="Italic">Crocuta crocuta</Emphasis>)

Avian models of facultative siblicide predict that rates of sibling aggression and the incidence of siblicide should be lower in prey-rich than prey-poor environments, and that siblicide should only occur when fitness benefits outweigh costs. We tested these predictions by comparing data from spotted hyena (Crocuta crocuta) twin litters in the Ngorongoro Crater, Tanzania, a habitat with a high density of resident prey (176 animals/km²) with similar data from the adjacent Serengeti National Park where density of resident prey is low (3.3 animals/km²). As predicted, rates of sibling aggression in Crater twin litters were substantially lower than those among twin siblings in the Serengeti. There was no evidence of siblicide in the Crater, in contrast to the Serengeti, where facultative siblicide occurs frequently. The growth rate of Crater cubs in singleton litters was similar to that of cubs in twin litters, whereas the growth rate of Serengeti singletons was higher than that of cubs in twin litters. Thus despotic behavior by dominant Crater cubs was unlikely to provide fitness benefits, while dominant Serengeti cubs that eliminated their sibling benefited from increased growth and enhanced survival. Previous studies have demonstrated biases in the sex-composition of hyena litters due to facultative siblicide. No such biases were apparent in Crater litters. Our results provide strong evidence that levels of sibling aggression in spotted hyenas are adjusted in an adaptive manner, and that siblicide is facultative and resource dependent. Our results do not support the idea of pre-natal manipulation of offspring sex by female spotted hyenas in response to changes in resource abundance.     

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.     

Honest begging in the blue-footed booby: signaling food deprivation and body condition

To determine whether solicitation by blue-footed booby chicks accurately encodes their need for food, we independently manipulated the body condition and recent food ingestion of singleton chicks and recorded three measures of begging. Variations in the three measures of begging covaried only partially, but in general, chicks begged more intensely when they were in poor body condition and also when suffering recent food deprivation. Effects of body condition and recent food deprivation on begging were broadly additive, although deprived chicks in poor condition failed to beg more intensely than those in good condition. Protracted short-term deprivation may create such a high level of need that the body condition component of need becomes temporarily unimportant. Parents more frequently fed chicks that begged more intensely, chicks in poor condition, and chicks suffering food deprivation. Deprived chicks in poor condition received more food than deprived chicks in normal condition even though they did not beg more intensely, possibly because parents responded not only to current begging but also to begging earlier in the day, or to other cues to body condition. These results support the hypothesis that begging of boobies represents honest signaling of need.     

Begging behavior and food acquisition by brown-headed cowbird nestlings

Understanding the selective forces that limit the exaggeration of begging signals is a critical issue in understanding the evolution of begging behavior. I studied the begging behavior of nestlings of the brown-headed cowbird (Molothrus ater), a brood parasite. In the nests of indigo buntings (Passerina cyanea), brown-headed cowbird nestlings received approximately twice as much food per hour than their host nestmates. I tested three hypotheses for the mechanism by which cowbirds acquired more food than their bunting nestmates: the size advantage hypothesis, the signal exaggeration hypothesis, and the novel begging behavior hypothesis. I found support for the hypotheses that cowbirds acquire more food as a result of their larger body size, and due to the exaggeration of begging signals that are not dependent on body size. I did not find support for the role of novel begging behaviors in cowbird food acquisition. These results suggest that food acquisition by host chicks in unparasitized nests could be increased by the exaggeration of begging signals. Recent work suggests that such exaggeration may be limited by the risk of nest predation, but further studies are needed. Received: 12 December 1997 / Accepted after revision: 29 December 1997