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.     

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     

The role of hatching asynchrony in siblicidal brood reduction of two booby species

Summary Hatching asynchrony (HA) of masked boobies (Sula dactylatra) in the Galápagos Islands differs from that of its sympatric congener, the blue-footed booby (S. nebouxii), in association with differences in brood reduction systems. Masked booby nestlings are obligately siblicidal, have long HA, and the probability and timing of siblicide is strongly influenced by HA. Blue-footed boobies are facultatively siblicidal and have shorter HA. Experimental shortening of masked booby HA demonstrated that this species maintians its HA above an early reduction threshold, below which parents may incur costs of provisioning a brood that they cannot raise to fledging, but that blue-footed booby HA occur above, at, and below the masked booby threshold. Differences in HA alone cannot explain the differences between these two brood reduction systems.     

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).     

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.     

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     

Parent-offspring cooperation in the blue-footed boody (Sula nebouxii): social roles in infanticial brood reduction

Summary Reproduction in the blue-footed boody was examined for evidence of parent-offspring conflict over infanticidal reduction of the brood. Parental investment was analysed by measuring clutch characteristics, and chick growth and mortality in four seasons. Direct observations were made of behavioral development to determine the social roles of family members. The modal clutch was two similar-sized eggs, which hatched 4.0 days apart due to a 5.1-day laying interval and immediate incubation of the first egg. On average, senior chicks grew faster than their sibs in years of good or poor growth (Fig. 2), maintaining the initial size disparity for at least 65 days (Fig. 1). Differential mortality of junior chicks was associated not with poor personal growth, but with a 20–25% weight deficiency of the senior sib, implying siblicidal brood reduction triggered at a weight threshold. Senior chicks established behavioral dominance through low-frequency pecking, but ordinarily did not eliminate their sibs nor substantially suppress their begging (Fig. 3), even when their own growth was 16% below potential. Parents fed dominant chicks more frequently than subordinates, but did not intervene in inter-sib aggression, even when it reached a siblicidal level. The weight and possibly the dominance relation between sibs was inverted in 12% of pairs. The theoretical prediction of conflict over elimination of the junior chick was not supported; rather, parents and senior chick cooperate, as if their fitness interests were congruent. Further, provisional tolerance of the junior chick by its underweight senior sib is consistent with self-sacrifice to increase the latter's inclusive fitness.     

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     

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     

Is kin cooperation going on undetected in marine bird colonies?

In multitudinous breeding colonies, kin interactions could go unnoticed because we are unaware of the kinship among adults we observe. Evidence of cooperation and competition between close adult kin in a blue-footed booby colony was sought by analyzing patterns of natal dispersal and proximity of nests. Male and female recruits nested closer to their own natal sites than to their parents’ current sites. Males (only) dispersed less far when both parents were present than when no parent or one parent was present, but not selectively close to fathers versus mothers when these were divorced. Neither parental presence nor parental proximity affected breeding success of recruits of either sex. Although distances between the nests of simultaneously recruiting broodmates were unrelated to their sex, males dispersed 13.1 m less when a sister was present than when a brother was present. Neither sex was affected in its dispersal distance by the presence or hatching order/dominance of a broodmate. Neither sex was affected in its breeding success by the presence versus absence of a broodmate, although female success increased with proximity of their brothers. Parents and sisters may actively or passively help males establish their first territories near their natal sites and nearby brothers may help females in their first breeding attempts; otherwise, boobies do not influence each other’s natal dispersal and first breeding success. It appears that boobies do not nest selectively close to or far from their parents, offspring, or broodmates. Why there is apparently so little cooperation and altruism between close adult relatives in booby colonies is puzzling.     

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.     

Interactive effects of male and female age on extra-pair paternity in a socially monogamous seabird

Females sometimes obtain older sires for their offspring through extra-pair interactions, but how female age influences paternity is largely unexplored and interactive effects across the age span of both sexes have not been analyzed. To test whether female choice of sire age varies with female age in the blue-footed booby (Sula nebouxii), we examined associations between ages of both partners and the probability of extra-pair paternity (EPP) in 350 broods of parents up to 22 years old in a single breeding season. Extra-pair paternity enables a female to select an alternative sire for her offspring and could function to avoid or achieve particular combinations of parental ages. A male age?×?female age interaction revealed that in young females (≤4 years), EPP decreased with increasing age of the social partner, whereas in old females (≥8 years), it increased. Moreover, sires of extra-pair (EP) chicks of young females paired to young males were on average 6.33 years older than the females’ social partners. Since female boobies control copulatory access, this pattern could imply that young females choose old sires for their proven genetic quality and that old females avoid very old males because matings with them may risk infertility or genetic defects in offspring. Taking female age into account and observing across the whole age span may be necessary for understanding female age-based mate choice.     

Hunger and food allocation among nestlings of facultatively siblicidal ospreys

Summary Previous studies of food allocation among nestlings of siblicidal birds have focussed on the proximate link between food and aggression. However, food sharing among sibs (and brood reduction) need not involve aggression. Here I examine the role of hunger (defined operationally in terms of the amount of food eaten recently) within the broader framework of passive and aggressive food-sharing among nestlings of facultatively siblicidal ospreys (Pandion haliaetus). Feeding among brood members was hierarchical; senior, dominant sibs ate more when hungry, leaving a smaller residual share of food for junior sibs. Senior sibs did not become more generous at large meals (i.e., the prospect of a large meal did not quell the selfish tendencies of senior sibs). That individuals ate more when hungry indicates a proximate link between food and the allocation of resources among siblings. Overall, aggression was infrequent and seemed to be used when junior sibs contested food allocation at meals. Aggression was diminished and food allocation was skewed toward the junior sib in broods with artificially exaggerated hatching intervals, suggesting that senior sibs were more generous when their dominant status was not threatened.Offprint requests to the present address     

Stable isotope ratios of a tropical marine predator: confounding effects of nutritional status during growth

Stable isotope analysis of carbon and nitrogen is frequently used to study the diets and foraging ecology of marine predators. However, isotopic values may also be affected by an individual’s nutritional status and associated physiological processes. Here, we use C and N stable isotopes in blood and feathers of blue-footed booby chicks at the Galápagos Islands to examine how isotopic values are related to body condition and growth rate, and to assess the consistency in the isotope ratios of individuals during growth. Size dimorphism in blue-footed boobies provided an additional opportunity to examine how isotope ratios differ between sexes in relation to body size and growth rate. There was no significant difference between sexes but both C and N stable isotopes were significantly negatively related to the body condition of chicks. These data were consistent with individual variation in physiological processes affecting fractionation, although we cannot rule out the possibility that they were also influenced to some extent by population-level variation in the stable isotope ratios of prey fed to chicks, for instance related to prey size, depth or lipid content. Our results highlight the need for methods that take proper account of confounding physiological factors in isotopic studies of foraging ecology and diet.     

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.     

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.     

Age-dependent effects of carotenoids on sexual ornaments and reproductive performance of a long-lived seabird

Understanding the mechanisms mediating age-dependent reproductive effort in wild animals is a major challenge in evolutionary ecology. The acquisition of molecules able to deter somatic damage could potentially improve reproductive performance, especially in physiologically compromised individuals. Carotenoids are antioxidants and immunoenhancers that animals can only obtain through diet. We tested in male blue-footed boobies whether carotenoid supplementation during incubation improves condition and reproductive performance, particularly of older males. Old birds showed lower levels of peroxidative damage than middle-aged males; however, changes of males' antioxidant capacity and peroxidative damage were not affected by carotenoid supplementation irrespective of age. Experimental old males displayed more colourful feet than control old males after 13 days of first carotenoid supplementation. The effect of carotenoids on male reproductive performance was dependent upon age: young males receiving extra-carotenoids produced chicks with smaller growth rates than control young males, whereas old males receiving extra-carotenoids produced chicks with higher growth rates than control old males. Our results highlight that carotenoids influence the relationship between age and reproductive performance and suggest a positive effect of carotenoids on reproduction of old males.     

Maternal investment in eggs is affected by male feet colour and breeding conditions in the blue-footed booby, <Emphasis Type="Italic">Sula nebouxii</Emphasis>

Females are expected to vary investment in offspring according to variables that may influence the offspring fitness in a way that optimises her inclusive fitness for a particular context. Thus, when sexual ornaments signal the quality of the male, females might invest in reproduction as a function of the attractiveness of their mate. We tested whether breeding conditions and male feet colour influence reproductive decisions of blue-footed booby females. In the blue-footed booby, male feet colour is a dynamic condition-dependent sexually selected trait that is related to paternal effort. During two consecutive years, an El Niño year (poor breeding conditions) and a year with good breeding conditions, we experimentally reduced male attractiveness by modifying their feet colour after the first egg was laid and recorded female investment in the second egg. We found that, relative to the first egg in the clutch, females laid heavier second eggs during the poor year than during the good year. Females paired with males with duller feet colour reduced second-egg mass and volume and delayed the laying of the second egg, independently of the year. Absolute yolk androstenedione (A4) concentration (but not testosterone, T) in second eggs was higher during a poor year than during a good year. Only during a year with poor breeding conditions, females paired with experimental males decreased the relative A4 concentration (but not T) in the second egg compared to control females. Thus, blue-footed booby females probably favour brood reduction by decreasing egg quality and increasing size asymmetry between chicks when the breeding and the mate conditions are poor.     

Tactics, effectiveness and avoidance of mate guarding in the blue-footed booby (Sula nebouxii)

We examined the dynamics and avoidance of mate guarding, by males and females, in the blue-footed booby, in which the two social mates are usually simultaneously present on the territory but each of them is unmonitored by the other for one-quarter of its time. Both sexes were promiscuous and liable to switch mates. Cuckolded individuals did not increase their overall presence on the territory, but in response to the extra-pair (EP) courtships of their mates, both sexes doubled their rate of intra-pair (IP) courtship and sometimes showed aggression. The male or female's presence depressed the social mate's EP activity, but intra-pair courtship had no such effect, tending even to propitiate that EP activity. Similarly, when females responded to their social mates' EP courtship with approach or aggression, disruption of EP activity was short-lived. Promiscuous females modified their diurnal pattern of attendance, as if attempting to sidestep monitoring by their mates, but cuckolded males matched the modification. Both sexes tended to perform their EP activities at a distance when their mates were present, possibly to evade monitoring or disruption by their mates. Male and female boobies cannot monitor their mates continuously, they do little to facultatively adjust their presence on territory to the risk of infidelity, and their immediate responses to overt infidelity have only the briefest impact; but the information they acquire while monitoring their mates may be critical to constraining their mates' infidelity and also to calibrating their own reproductive investment.     

Benefits of large broods by higher chick survival and better territories in a precocial shorebird

When reproductive success is constant in one breeding phase, different tactics that increase variation in reproductive success among individuals may evolve in other phases. For instance, in shorebirds, which usually have a limited clutch size of four eggs, variation in reproductive tactics among individuals is expected either before egg-laying (e.g. diverse mating systems) or after hatching of the young (e.g. diverse parental care). In this paper, I studied the pied avocet (Recurvirostra avosetta), a shorebird with a modal clutch size of four eggs, to test whether post-hatch chick adoption as an alternative tactic can be linked to increased variation in annual reproductive success. When predation was high, naturally adopting pairs produced more filial fledglings than did pairs not adopting chicks and not losing chicks to adoption. The number of filial fledglings increased with the number of adopted young, possibly through diluting the chances of predation on filial young. Experimental chick addition did not lead to more fledged young due to low brood integrity as shown by the frequent loss of chicks from some experimental broods. When predation was low, larger broods occupied feeding territories with higher prey abundance than smaller broods, possibly due to their dominance over smaller ones. Pairs that lost chicks to adoption (donors) fledged as many filial young in their broods as did non-adopters/non-donors, whereas the total number of donors’ filial fledglings, including those raised in adopting broods, approached that of adopters. These findings show, for the first time, that post-hatch alternative reproductive tactics can lead to variation in annual reproductive success and to higher success for some pairs even in species where past adaptations limit variation in reproductive success in a certain phase of reproduction.