S28.5: Agonism and dominance in nestling birds

Instituto de Ecología, Universidad Nacional Autónoma de México, A.P. 70-275, 04510 D.F., Mexico, e-mail hugh@servidor.unam.mx

In species of birds where aggression among nestlings results in siblicide, the agonistic relationship between nestmates varies from unrestrained violence to ritualised dominance-subordinance. Three types of dominance could be involved: true dominance, trained winning and losing, and asymmetry of attributes. Field experiments have shown that in broods of two Blue-footed Boobies, dominance by asymmetry of attributes soon gives way to trained winning and losing. Training of junior chicks as losers is associated with elevated circulating corticosterone, apparent debilitation, and more persistent behavioural effects than training of seniors as winners. Nonetheless, subordinate chicks monitor the relative size and aggressive potential of their nestmates, and sometimes rebel when they detect an advantage. We have little idea of how the three types of dominance are distributed among other species of birds, or how they affect behavioural development. Sibling agonism is potentially a source of individual behavioural differences among adults.

Over the last 20 years a number of field studies have explored the dramatic phenomena of aggressive competition among avian nestlings. This work was inspired by selection thinking and in particular the theoretical approaches to within-family conflict and co-operation of Hamilton (1964a, b), Trivers (1974), O'Connor (1978) and Parker (Parker & Macnair 1978; Macnair & Parker 1978). The main aim has been to elucidate the adaptiveness of social behaviour involved in obligate and facultative brood reduction: unconditional and conditional siblicide (e.g. Mock et al. 1990). The general approach has been to describe the social interactions of siblings and their parents and analyse with experiments the ecological and social factors that influence aggression as well as its effects on growth and survival of nestlings. The precise psychological nature of the relationship between siblings has not been a focus of attention, but most field workers have used the word ‘dominance’ to describe it.

‘Dominance’ is something of a psychologists' old chestnut, and although the term is still widely used by students of animal behaviour, it is variously understood and still controversial. Dominance can mean simply that there is a consistent asymmetry in the agonistic relation between two individuals (e.g. Dewsbury 1982), or more restrictively it refers to predictable asymmetry due to effects of previous experience on their behavioural tendencies. Dominance among infant birds apparently affects their food allocations, growth and mortality (e.g. Mock 1985; Osorno & Drummond 1995), although the causal link has not been demonstrated experimentally; and has the potential to produce longer-term effects on behavioural development. Here, after briefly discussing the concept of dominance, I review descriptive and experimental studies that provide a partial portrait of sibling dominance in young Blue-footed Boobies Sula nebouxii and draw attention to our ignorance of developmental consequences beyond fledging. I also suggest that experimental analysis of natural dominance relationships among members of vertebrate broods and litters is rare and potentially offers a key to a major problem in animal behaviour: the ontogeny of individual differences.

The concept of dominance was extensively probed after the early 1920's when researchers discovered that groups of adult birds, mammals and other animals often organised themselves according to an agonistic hierarchy (e.g. Schjelderup-Ebbe 1922). ‘Peck orders’ and ‘rank orders’ were major organising features, and they specified systems of preferential rights enforced by aggression and acknowledged by submission and deference (Allee 1942). Thus, individual competition for such resources as food or access to females was mediated and moderated by conventional behaviour. Correlates of dominance such as sex, body size, seniority in the group, and hormones were discovered, and hormone levels and agonistic experience were shown to affect the development of dominance status. After the 1960's research effort declined when disillusion set in as it was realised that the idea of a linear rank order can be overly simplistic and that direction of dominance between two individuals varies with the situation (Schein 1975). Hierarchies themselves might not be properties of groups of animals but inventions of observers. It was even doubted whether dominance is a useful concept if the determining feature of a bilateral relationship is the submissiveness of one individual rather than the aggressiveness of the other; maybe the essence of the relationship is subordinance (e.g. Rowell 1974).

Subsequently, Bernstein (1981) defined and cogently defended the concept of dominance, as applied to dyadic relationships, as well as defining other, similar relationships (which he did not recognise as types of dominance). Drews (1993) provided further analysis and categorization. Here, I refer to Bernstein's four categories as ‘true dominance-subordinance’, ‘territorial dominance’, ‘trained winning and losing’, and ‘asymmetry of attributes’. A true dominance relationship arises when a history of interactions between two individuals results in one of them habitually performing submissive responses at the outset of encounters with the other specific individual; this relationship depends on individual recognition. Territorial dominance occurs when similar predictability between two animals depends not on their individual identities but on spatial location of the encounter (e.g. Kaufmann 1983). Trained winning and losing also depends on learning, but does not involve individual identity or location: when a history of wins or defeats makes an animal habitually aggressive or submissive to other conspecifics generally, then it is a trained winner or loser, respectively.

Finally, it is commonly stated in relation to particular species that males dominate females (or vice versa), that adults dominate juveniles, or that one colour morph dominates another, and so on; in the sense that sex, maturity, and such variables predict which individual will yield in confrontation or competition over some resource. Such predictable interactions between classes of conspecifics reflect asymmetry in attributes. In principle, they could arise from previous experience or innate tendencies.

In all four categories the term dominance is invoked because one of two contendents yields; that is, emits a response that terminates the aggressive interaction (reduces the probability of aggression by the other animal), for example, by fleeing, stepping back, crouching or performing a submissive display. Bernstein's definition of true dominance requires that yielding occur at the outset of the interaction. Indeed, in all four categories if yielding does not occur early on, then what we probably have is not dominance/subordinance but predictable victory in an unequal contest.

Three of the above four categories of agonistic dominance may be applicable to the offspring of birds. No author has hitherto suggested that territorial dominance might be relevant to avian nestlings nor reported observations that would support such an interpretation. True dominance is a plausible candidate, although I am not aware of any study that makes a case for individual recognition among nestlings. Typically, asymmetry in attributes has been invoked by students of aggressive brood reduction; we are told either that one member of a dyad habitually prevails over the other because it is older and larger (e.g. Edwards & Collopy 1983; Bortolotti 1986a, b), or that, exceptionally, the more junior (younger) chick prevails despite smaller size because it happens to be stronger or more vigorous. If the loser yields early on in a nestling interaction, then this is probably dominance governed by asymmetry of attributes; if, however, both fight it out and one loses because it is outmatched, then there is simply an unequal agonistic contest and dominance, as defined above, is not involved. Learned winning and losing could well be involved in some species. This behavioural phenomenon was demonstrated in the early days of dominance research on adult rodents, albeit often without proper controls (e.g. Ginsburg & Allee 1942; Scott & Marston 1953), and it was later shown to occur in experimental pairings of birds (Ratner 1961) and lizards (Zucker & Murray 1996). Again, controls have usually been inadequate, and the natural context of the behaviour has seldom been specified, but in the case of three species of fish it now seems likely that repeated experiences of winning and losing can result in an animal habitually adopting an offensive or defensive role, respectively, in relation to new opponents (Beaugrand & Zayan 1985; Frey & Miller 1972, Beacham & Newman 1987, Chase et al. 1994). In principle, such training of a nestling could make it routinely respond to a nestmate by either asserting itself or yielding. In broods of three or more nestmates a slightly finer process of generalisation and discrimination could create a linear hierarchy, with intermediate chicks learning, say, to attack any individual that is larger and defer to any that is smaller.

In most avian species competition among broodmates occurs through begging competition rather than agonism; chicks jostle for position, display to parents and strive to receive proffered food (e.g. Redondo & Castro 1992, Anderson et al. 1993). In the minority of species where facultative or obligate brood reduction occurs through sibling aggression, agonistic interactions vary greatly (review in Mock & Parker 1997). Three examples will illustrate the diversity in aggressive and defensive strategies, communication between contenders, and the possible importance of learning.

In the Matopos, Zimbabwe, Black Eagles Aquila verreauxii usually lay two eggs, but the first-hatched chick, which is four days older, always kills its nestmate by direct aggression combined with induced starvation within several days (Gargett 1978). In one nest, the senior chick started attacking its sibling 15.5 h after the latter hatched, then mounted repeated assaults until it died three days later. It pecked forcefully at any part of the body as well as gripping the junior chick's rump and pulling out beakfuls of down. Death occurred after the junior chick steadily lost weight and suffered multiple wounds in the course of receiving 1569 pecks. It was pecked whether it was attempting to feed, moving about or simply lying still. On day one the junior chick pecked its sibling once, but this may have been feeding behaviour. After the first 48 h of punishment this chick no longer faced its nestmate with erect stance and seldom raised its head. There was never any other indication of submissiveness by the junior chick and Gargett concluded that it was not intimidated.

Great Egrets Casmerodius albus in typical three-chick broods hatch at one- or two-day intervals and brood reduction is facultative, with survival of the younger chicks apparently dependent on the amount of food provided by parents. Chicks fight about five times a day, starting within days of hatching, even though fights at this stage do not appear to influence food distribution (Mock & Parker 1997). Fighting occurs during and outside feeding bouts and is not ritualised; mostly chicks jab at each others' faces and heads, exchanging blows until one of the pair concedes by crouching low, fleeing or hanging it's head outside the nest. Then the victor may desist or continue pecking for a while, sometimes pursuing the victim or grasping and slamming it against the nest cup. By the time direct beak-to-beak parental feeding predominates (at roughly 14 days), the brood shows a stable, linear agonistic hierarchy, with the most junior chick in particular frequently declining to contest aggression by pecking back. This chick appears ‘intimidated’ as a result of cumulative earlier beatings, and its consequent hesitancy or failure to beg and reach for food results in it getting less food and growing more slowly than its sibs (Mock 1985).

In three- and four-chick broods of the Western Grebe Aechmorphus occidentalis, chicks hatch at one-day intervals and within 5-15 min climb beneath the parent's wing, where they are fed by the other parent (Nuechterlein 1981). Intense pecking among nestmates during the hatching period results in an agonistic hierarchy: senior chicks peck severely and threaten vocally, and junior ones turn away and hide. Subsequently, as nestlings cruise around on the back of one parent, the physical proximity of a senior chick inhibits a more junior chick from emerging from the feathers in response to the parent's calls. Rather than emerging from the feathers to receive food, it begs furtively and receives nothing until the senior chick is satiated.

No experiments have analysed the types of dominance relationship in these three species, but the agonistic roles differ: in Black Eagles, senior chicks are unrestrainedly violent and juniors unsubmissive but usually overwhelmed and cowed; in Great Egrets, seniors may be somewhat restrained in their aggression and juniors are unsubmissive and although often cowed they frequently fight back; in Western Grebes, early one-sided violence is soon substituted by communication: threats and submission. This could represent some sort of continuum from simple unequal contests (without dominance) in the Black Eagle, and possibly the Great Egret, to learned winning and losing or even true dominance in the Western Grebe.  It has been suggested that the most important function of aggression among very young nestlings may be agonistic training rather than immediate food competition (Mock 1985; Drummond & Osorno 1992; Pinson & Drummond 1993), but function seems likely to vary among species.

The Blue-footed Booby lays one to three eggs in a scrape on the ground, on small islands in the eastern Pacific Ocean. Broods of one, two or three chicks hatch with intervals of roughly four days between them, and both parents feed them for four months or more by regurgitating sardines and anchovies into their mouths (Nelson 1975). Throughout this period, all broodmates manifest conspicuous dominance-subordination. In broods of two, the senior chick attacks and threatens its nestmate daily and the latter responds with the bill-down-and-face-away (BDFA) posture that is thought to inhibit further aggression (Drummond et al. 1986).

The senior chick has a better chance of surviving to fledge than the junior one, in part because it has privileged access to food. For example, on Isla Isabel, Mexico, seniors receive 26% more feeds than juniors (probably representing about 20% more grams of fish) in each chick's first week of life, and continue to receive a larger share during at least the first 5 weeks (Guerra & Drummond 1995). However, in broods where both chicks fledged, although junior chicks were on average 11% lighter than their sibs when both were 20 d old (Drummond et al. 1986), they eventually caught up: by the time they were nearly fully feathered at 79 d, juniors and seniors were similar in size and weight (Drummond et al. 1991). In 447 broods observed from hatching, junior chicks were 26% more likely than seniors to die before fledging (55.3 vs 43.9% died, respectively), and deaths could occur at any time during at least the first 10 weeks of life (Drummond, unpublished data). Most deaths were attributed to starvation, or expulsion from the nest followed by infanticidal attacks of colony neighbours.

Aggression involves stabbing the victim's head, nape and body with closed or nearly closed mandibles, grasping and twisting the skin, and emitting harsh vocal threats. The average senior chick pecks only 2.9 times per day during the first 60 days, pecking most frequently at age 10-20 d, when its sibling is 6-16 days old (Drummond et al. 1986). At age 10 d it has acquired sufficient motor co-ordination to deliver telling pecks and its nestmate is emerging from under the parental breast feathers often enough to make an accessible target. In stark contrast, the average junior chick pecks only 0.1 times per day in the first 60 d, mostly when it is 5-10 d old. This sorry struggle to take the offensive is soon substituted almost completely by submissiveness, and junior routinely adopts the BDFA posture and/or moves away from its nestmate when threatened or attacked.

Volleys of vigorous pecks and bites to the head, nape and eyes look dangerous, but seldom cause visible lesions. Aggression occurs both during and independently of feeding bouts, and while it sometimes conspicuously suppresses begging and feeding by the subordinate chick at critical moments, it can also be suspended during a feeding bout, allowing junior to feed even when senior is begging alongside (personal observation). This and other observations have led two independent teams to infer that senior chicks tolerate food-sharing despite having the physical capacity to marginalise their nestmates more than they customarily do (Drummond et al. 1986, Anderson & Ricklefs 1995).

Even so, food shortage can be a powerful stimulus for aggression, and may be the principal cause of intensified pecking and siblicide. Senior chicks that lost their sibs were found to be underweight compared with their peers and roughly 20-25% below their potential weight, on the day before loss (Drummond et al. 1986). And in broods artificially deprived of food, pecking by seniors increased severalfold, reaching maximum values on the day when their weight deficit was roughly 20-25% (Drummond & García Chavelas 1989). In experimentally paired chicks, relative food deprivation can determine which one becomes aggressively dominant (Rodríguez-Gironés et al. 1996). Female boobies grow faster than males and by age 79 d they are 27% heavier. Such size dimorphism is expected to tip the scales of sibling competition in favour of females (e.g. Craighead & Craighead 1956; Edwards & Collopy 1983; Edwards et al. 1988). Yet longitudinal observations of brother-sister dyads showed no effect of relative size on competition, either in broods where the female hatched first and was always about 30-135% heavier than her nestmate on average, or in broods where she hatched second and overtook him at an average age of 37 d (Drummond et al. 1991). Surprisingly, sex of the nestmate did not affect a chick's survival or, in broods where both chicks fledged, its growth schedule or attainment, be it male or female, senior or junior. And this may be partly due to the longitudinal stability of the agonistic relationship: dominance was inverted during the nestling period in only one brood of 54 (including 27 broods that suffered no mortality and were observed until chicks were an average 118 d old). Particularly striking was the continued dominance by males of the younger sisters who outgrew them and eventually become an average 21% heavier than them.

This longitudinal stability in brother-sister agonism seemed to contradict the expectation of differential size determining the winner (either through simple unequal contests or due to dominance in response to asymmetrical attributes).  Stability seemed very likely to be due to learning, implying a relationship of true dominance or trained winning/losing.

To test whether early experience influences tendencies to behave aggressively or submissively, Drummond & Osorno (1992) established experimental pairs of 12-55-d-old chicks, either in artificial nests or by swapping chicks between natural nests. Each one had grown up as a Dominant or Subordinate in its natal two-chick brood. As predicted, in these 30-min or 4-h trials each chick behaved as it had behaved in the natal nest, no matter whether its (unfamiliar) nestmate was a Dominant or a Subordinate. Thus, in experimental pairs of Dominant and similar-sized Subordinate, the former was aggressive and non-submissive and the latter vice versa. In pairs of two Dominants, there were series of escalated battles, involving temporary exhaustion and submission of losers followed by renewed assaults on or by winners. In pairs of two Subordinates aggression was absent or minimal.

Nonetheless, it seemed likely that in the absence of social experience with a sibling, relative size would determine direction of dominance, and this was tested by pairing Singletons from natural broods of one chick. In these 4-h trials, a dominance-subordinance relationship emerged promptly and in nearly every pairing it was the larger chick that adopted the dominant role. Even when the difference in size was very small, both chicks readily detected and respected it. Clearly, these Singletons were responding to an asymmetry in some attribute; probably size, mass or an indicator of maturity.

What would chicks do when the dictates of previous learning and current attributes were opposed? This is the situation that emerges when a female chick outgrows her elder brother, although sex and age confound that natural test of influence of relative size. To answer this question, we formed experimental pairs of a Dominant and a Subordinate that was on average 32% heavier and 3.9 d older, and compared them with control pairs where chicks were fostered similarly between nests while maintaining the natural size and age asymmetry of dominant and subordinate nestmates (Drummond & Osorno 1992). Chicks were 15-31 d old.

In this test, effects of previous learning proved to be paramount, but it was also clear that relative size/age/maturity simultaneously exerted an important influence on the behaviour of Subordinates. During the first three days, 11 of 12 experimental Dominants pecked more frequently than their larger nestmates. Experimental Subordinates were more aggressive than control Subordinates (which did not peck at all), eight of them challenging their suddenly smaller nestmates by aggressive pecking. However, despite their new pugnaciousness and willingness in some cases to do battle over several days, only one of them eventually prevailed; their aggressiveness provoked intensified attacking by the small Dominants (greater than by control Dominants), and they themselves seemed overly ready to submit when attacked. One experimental Subordinate sustained a high level of aggression during at least 6 d, frequently eliciting submission from the Dominant, although overall it pecked less frequently. This Subordinate started out 62% heavier and 5 d older than its rival, and persisted in making periodic attacks during at least 5 weeks but never established supremacy. It seems that chicks are conditioned by a subordinate role in the natal nest to behave submissively, but continuously assess their nestmate's relative size or strength and attempt to aggressively invert dominance if they sense a favourable asymmetry. However, during such a mutiny they seem handicapped by a strong tendency to capitulate, and by their dominant nestmate's tendency to escalate after being attacked. Hence, natural dominance inversions tend to occur through a process of agonistic attrition extended over many days (e.g. 16 d, in Drummond et al. 1991).

The above experimental results imply learning, but they could have been due to Dominants learning to be more aggressive than Singletons (the baseline agonistic condition) or to Subordinates learning to be more submissive than Singletons. We tested these two hypotheses by permanently pairing Dominants with Singletons that were slightly larger, and Subordinates with Singletons that were slightly smaller (Drummond & Canales 1998).

During the first four hours, Dominants were six times as aggressive as Singletons, and Subordinates were seven times less aggressive than Singletons, clearly showing that both were sufficiently affected by early experience for learning to overrule relative size. Then, over the medium term, a difference emerged: Subordinates sustained their subordinate role over and beyond 10 d of continuous cohabitation, whereas by day six only half of Dominants were outpecking their Singleton nestmates. Thus, in our experimental situation, training as a loser produced a more persistent effect than training as a winner. However, our testing situation tended to reinforce subordinate training and reverse dominant training, so we should be cautious about concluding that subordinate training produces effects that are more resistant to reversal.

Interestingly, there was evidence that dominance relationships in Dominant-Singleton pairs were unstable during at least four weeks. The chick that customarily assumed the subordinate role was not as compliant as junior chicks in natural pairs, presumably because it had not been similarly exposed to consistent intense aggression during its first three weeks of life. Chicks were 13-20 d old when they were paired for the experiment.

The aggressiveness of Singletons paired with slightly larger Subordinates in the last experiment seems to contradict our earlier conclusion that chicks lacking experience with siblings allow relative size to determine their agonistic posture. We suspect that shortly after pairing, these Singletons detected the experimental nestmate's habitually submissive demeanour, and responded with aggression. This would imply that chicks continually assess not only relative size but also some (behavioural) index of their nestmate's agonistic tendencies or potential.

The pioneers of research into dominance hierarchies in adult animals uncovered hormonal correlates of status and showed that sex hormones, in particular, can affect position in a hierarchy (e.g. Allee et al. 1939). More recent research focussed on natural contexts has shown that although elevated levels of testosterone facilitate aggressive behaviour in adult birds, artificial testosterone boosts frequently are insufficient to overcome effects of social conditioning (Rohwer & Rohwer 1978; Ramenofsky & Gorbman 1980). The Challenge Hypothesis sustains that testosterone remains at a low level in stable agonistic relations, and secretion increases to support aggressive intensification when a dominant animal responds to a threat to its privileged status (Wingfield et al. 1990). Nestling birds can show high levels of circulating sex steroids (Hutchison et al. 1984; Marler et al. 1987), so it is possible that elevated testosterone facilitates nestling dominance. It is also possible that elevated corticosterone could facilitate submissiveness in subordinate nestlings, since it does so in some adult vertebrates (Leshner 1981, 1983).

We made an exploratory test for endocrine correlates of agonism in blue-footed booby chicks by measuring circulating hormones in 15-20-d-old broods of one and two chicks undergoing artificial food shortage, induced by taping their necks to prevent ingestion of parental feeds during 48 h (Nuñez de la Mora et al. 1996). Such food limitation had previously been shown to result in a substantial increase in aggressive pecking and threatening by the dominant chick of a pair (Drummond & Osorno 1992).

Testosterone was not detected in any blood sample, either before or after food limitation, implying that testosterone is not involved in the establishment of dominance nor in the young dominant chick's aggressive intensification in response to food shortage (see also Ramos-Fernandez et al., in press). However, baseline corticosterone level was twice as high in Subordinates as in Dominants or Singletons, consistent with this hormone possibly increasing with social subordination and even facilitating submissive behaviour. Further, corticosterone levels were higher after 48 h food deprivation in Subordinates, Dominants and Singletons, implying that secretion increases in response to frustration and starvation. The behavioural consequences of increased circulating corticosterone remain to be determined. Plausibly, this hormone makes Dominants more aggressive and Subordinates more submissive by facilitating their responsiveness to social stimuli.

In the behavioural development of pairs of Blue-footed Booby chicks, the early aggressiveness of both nestmates eventually gives way to trained winning and losing. In recently hatched broods, the elder bird quickly assumes a dominant role and its nestmate assumes a submissive role. Presumably it is asymmetry in size, mass or maturity that sets the direction of agonistic interchanges in the early days. Possibly at the very start both birds are equally inclined to attack and the relationship is one of predictable victories in unequal contests; but within days the junior chick readily signals submission with the BDFA posture. At first, this submissiveness may only signify a relationship of dominance through asymmetry of attributes, but by the time juniors reach age 12 d the senior chick is a trained winner and the junior chick a trained loser. Training is likely to involve both classical conditioning (Archer 1988:152) and operant conditioning by negative reinforcement (Drummond & Osorno 1992). But this may not be all. Conceivably, both the original agonistic relationship and the training process are also facilitated (or opposed) by maternally-provided hormones. In both Canaries Serinus canaria and Cattle Egrets Bubulcus ibis, mothers spike their eggs differentially with androgens according to laying order (Schwabl 1993; Schwabl et al. 1997), and in canaries the extra testosterone confers advantages in begging and growth (Schwabl 1996). It is also possible that individual recognition plays some role in regulating the agonistic tendencies of booby chicks; there may be an element of true dominance. However, a preliminary test of sibling recognition in 29-59-d-old chicks produced negative results (Drummond & Osorno 1992).

The pattern of agonism shown by the senior chick can be interpreted as a strategy to efficiently control the junior chick over the entire nestling period, at minimal cost. The functional importance of intensified early aggression (when senior is 10-20 d old and junior is 6-16 d old) may be that: (1) it is applied when asymmetries are maximal (e.g., senior is 50-135% heavier than junior; Drummond et al. 1991, Fig. 2) and resistence can be crushed; and (2) it disables junior's aggressive potential to a degree that might be impossible later on. When Dominant/Singleton pairs were formed at age 13-20 d, the dominance relationships they established proved to be unstable during at least four weeks. In the natural situation, the restrained aggression by seniors after reaching age three weeks may be set at the minimum necessary to prevent spontaneous decay of training effects; with just a few vocal threats and pecks every day (acknowledged by submissive postures), Subordinates remain submissive and Dominants aggressive. Restrained aggression by the dominant chick may normally be sufficient to contain any challenges by the subordinate one because it is combined with conditional intensification: attacked dominants respond to belligerence by escalating.

The pattern of agonism shown by the junior chick is complex, combining elements of acquiescence, vigilance and conditional intensification. It makes functional sense for a hatchling to submit to an overwhelmingly superior aggressor, even when this implies being trained as a loser. A submissive junior receives less physical punishment and it can count on its sibling eventually reducing attacks to a symbolic level (unless food goes short). It also makes sense for subordinate chicks to continuously monitor the relative size and the demeanour of their adversary, launching a mutiny only when the balance of aggressive potential tips in their favour and dominance can be wrested without excessive fighting.

Subordinance may not only be a role characterised by tendencies to submit and not attack; it may also involve reduced capacity for aggression. In our experiment (Drummond & Osorno 1992), most Subordinates suddenly confronted by a substantially smaller and younger nestmate apparently attempted to invert dominance, and seven of eight failed in their attempt. Possibly, these Subordinates were only probing, rather than deploying their full potential. But one of them, at least, seemed to make an all-out effort that lasted several weeks, yet its initial weight advantage of 62% proved insufficient to invert dominance. This suggests that training as a loser imposes debility. And the functional advantage of imposing debility would explain why young seniors sustain punishing attacks on their siblings over many days rather than responding to their first submissive displays by promptly shifting to a low level of ritual aggression. A cumulative, unavoidable effect of punishment is implied.

Assuming that punishment imposes debility, why have boobies not evolved the capacity to resist this effect? An allele for resistence surely would progressively replace an allele for weakness (even if this then set the scene for subsequent evolution of less restraint by Dominants), so it seems likely that there is some constraint on evolving resistance, possibly a physiological constraint associated with elevated corticosterone production.

It is too early to say whether trained winning and losing is likely to be widespread among the broodmates of other siblicidal avian species. Certainly it would be worth testing for similar processes in Brown Pelican chicks Pelecanus occidentalis, which also show elevated aggression early in nestling life and signal submission with the BDFA posture, although junior pelican chicks maintain a higher level of aggressive resistance than junior Blue-footed Boobies (Pinson & Drummond 1993). In species such as the Great Egret (Mock and Parker 1997), the Black Eagle (Gargett 1978) and the Brown Booby Sula leucogaster (personal observation), junior chicks seem only to cower, hide and flee to avoid further punishment, implying that no ritualised display could elicit restraint and that no dominance relationship exists. Possibly, thoroughgoing training of subordinates as losers will turn out to be a feature of species, like the Blue-footed Booby, where subordinate chicks have a very high probability of fledging along with their nestmates. Such chicks, having little to gain by outfighting their siblings, should comply with subordinate status. Dominant chicks faced with compliant siblings can reap the inclusive fitness benefits of allowing them to survive and thrive, safely restraining their own aggression so long as any potential threat can be neutralised in advance by debilitating it.

The post-fledging developmental consequences of roles in nestling agonism are unknown. It is certainly plausible that behavioural subordinance throughout nestling life, combined with elevated circulating corticosterone, would subsequently make a juvenile or adult Blue-footed Booby less competitive, affecting survival, territory acquisition and mating opportunities. It has even been claimed that the function of the Black Eagle's second chick is to serve as a sort of punchbag, on which the first chick can build and hone the dominance it will eventually need for success in competition with other adults (Simmons 1989, 1991). Just as sibling interactions have been shown to be an important influence on the development of human personality (Sulloway 1996), so could agonistic sibling interactions, particularly stable ones during infancy, be important shapers of individual differences in behaviour in other animals. Several authors have noted this issue (e.g. Clark & Ehlinger 1987) but, to my knowledge, there are no systematic data for any species of vertebrate that grows up in a brood or litter. A challenge will be to separate long-term effects due to social experience and learning from those due to differential growth and nutrition.

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