as possible, and their fledging success was assessed. Results. Dominance Hierarchy in Confined Broods. The weight of confined broods lagged behind that.
Behavioral Ecology and Sociobiology
Behav Ecol Sociobiol (1981) 9:59~53
9 Springer-Verlag 1981
Social Hierarchy Among Siblings in Broods of the Oystercatcher Haematopus ostralegus Uriel N. Safriel* Edward Grey Institute of Field Ornithology, South Parks Road, Oxford OX1 3PS, England Received November 17, 1980 / Accepted April 3, 1981
Summary. O n S k o k h o l m Island, Wales, the y o u n g o f the Oystercatcher (Haematopus ostralegus) are fully precocial, yet are totally dependent on parents for food. T h o u g h all y o u n g ( c o m m o n l y three) usually hatch within one day, small hatching intervals do exist, and first-hatched nestlings are usually slightly heavier at hatching than those hatched later. Firsthatched y o u n g a n d / o r initially heavier y o u n g become socially d o m i n a n t over their siblings; a stable, linear, non-aggressive social hierarchy a m o n g siblings develops, which determines the partition o f f o o d a m o n g them and results in unequal distribution when f o o d is scarce. F o o d shortage impairs the growth rate o f subordinate young. They are rather h u n g r y and restless and consequently predation on them is higher than on d o m i n a n t young. It is p r o p o s e d that Oystercatchers achieve effective b r o o d - r e d u c t i o n by the parents' control o f differential egg weight, by the eggs' hatching order, and by the y o u n g ' s acceptance o f a non-aggressive social hierarchy. The latter is an adaptation associated with the unusual p h e n o m e n o n of fully precocial wader y o u n g being exclusively fed by parents.
Introduction Sibling interrelations are often expressed in social hierarchies a n d / o r size hierarchies and frequently lead to b r o o d reduction. M o s t cases of social hierarchies within b r o o d s develop against a b a c k g r o u n d o f async h r o n o u s hatching, and a m o n g semialtricial (Meyburg 1974) and semiprecocial (Procter 1975) species, i.e. a m o n g birds whose y o u n g are confined to a small space where they are fed by parents. In these cases, * Present address: Department of Zoology, The Hebrew University of Jerusalem, Jerusalem, Israel
hierarchy is maintained by explicit and non-ritualized aggression, otherwise rare a m o n g birds. A case is reported here o f non-aggressive social hierarchy a m o n g fully precocial siblings that are fed by parents, but which hatch fairly synchronously. The social hierarchy o f Oystercatcher (Haematopus ostralegus) siblings and its manifestation in b r o o d - r e d u c t i o n is discussed first; its adaptive value is then examined.
Materials and Methods Observations were made on Skokholm Island in Wales during 1965 and 1966 (Safriel 1967). The eggs (usually three) hatch within one day, and the nestlings leave the nest a few hours after hatching and are dependent for food on their parents until fledging. During the first month they move between hiding places in their parents' territory and expose themselves only to be fed. Except at a very early age when they require considerable brooding, the young move, hide and feed mostly singly. Their behaviour is therefore very different from that of many fully precocial birds, in which the family acts as a tight group. In 1965, I erected canvas pens (10 x 5 x0.5 m) around four nests in incubation. The parents became accustomed to flying over the obstacle, and once the young hatched the parents fed and brooded them. Observations on the individually marked young were made from a hide. In 1966 observations on 13 unconfined broods were carried out with the aid of four portable hides. They were pitched at different parts of a given territory and were either used alternatively or were relocated to follow the movements of the individually marked young. The young were weighed as often as possible, and their fledging success was assessed.
Results
Dominance Hierarchy in Confined Broods The weight o f confined b r o o d s lagged behind that o f unconfined ones (Fig. 1 a), the f o r m e r showing apparent signs o f p e r m a n e n t hunger. All siblings rushed together towards the feeding parent, but the heaviest chick was faster in reaching the parent and in snatching food. As time went on, the distribution o f f o o d items a m o n g siblings became markedly uneven, m o s t
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Social Hierarchy in Unconfined Broods
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Fig. 1. a Growth of confined broods. Mean weight of a chick in a confined brood (solid curve, based on four broods) compared with that of a chick in an unconfined brood (dashed curve, based on four broods, each selected to conform with one confined brood, with respect to time of hatching, initial brood size, and food type). Box indicates growth of siblings in one confined brood, b Agedependence of the advantage of weight of the d o m i n a n t chick (expressed as the percentage difference between the a chick and its b sibling, ordinate) in four unconfined broods free of disease
items being eaten by the heaviest chick. Ferocious fights for food became common, and often two young pulled an item in a ' tug or war' fashion, while running frantically within the pen. Most combats ended in favour of the heavier chick, which then resorted to a shelter where it stayed motionless. The loser remained in the open, either begging vociferously, running along the pen's wall, or pecking the ground. After about day 10 the mean weight of a confined chick started to drop (Fig. 1 a), but that of the initially heaviest chick continued to increase (Fig. 1 a, box). It became apparent that the lightest chicks would starve to death, and pens were then opened.
In spite of weight differences among siblings, fights were very infrequent and only rarely did more than one chick rush to a food-carrying adult. In terms of priority of access to food, a stable dominance relationship existed within each brood so that in ten broods, each composed of two young, a always dominated b, and in the three broods of three young each, a dominated b and c, and b dominated c. The identification of each sibling's rank was achieved within 34 h of observation, during which several scores of food items were offered. There were two types of feeding. One type was characterized by the parent arriving with food at a specific location and uttering a typical note. The chick that then reacted with an immediate, unhesitant rush towards the parent was identified as dominant, whereas the one that peeped from its hiding and approached only if no other chick had emerged first, was identified as subordinate. Only when the dominant seemed replete and retreated to hiding did the next in rank emerge to be fed. In the second type, the young chick followed a foraging parent. If it temporarily left the parent to rush towards an approaching sibling, the former was identified as dominant and the latter as subordinate. If it hastily ceased following and retreated to hiding when sighting another chick, the former was identified as subordinate and the latter as dominant. Unfed subordinates often begged from the on-watch parent, but never from the one followed by the dominant. When two young were near a foraging parent, only the dominant was fed, whereas the subordinate kept a distance behind. When both parents were on territory, the dominant was fed by the parent that was habitually more active in young-feeding (Safriel 1967), whereas the subordinate begged and sometimes received food from the other parent. Only when the dominant chick retreated could the subordinate exchange parents. All identifications were checked several times before each of the 30 observation sessions terminated, so that broods were observed at several ages, and the hierarchies were usually found to be stable. Slight skirmishes and threat postures were occasionally noted: when a subordinate approached a dominant following a foraging parent, the dominant dashed forward, causing a swift retreat of the subordinate. Emergence of a dominant from hiding caused the subordinate to immediately hide, even without the presence of a parent in the territory. Dominance was also exerted by call notes: a dominant might emit a note when emerging from hiding, and this caused the subordinate to leave the foraging parent and be replaced by the dominant. In several cases,
61
the young were scattered within a cover of bracken. They were fed in a bare patch to which they moved in response to a call of the parent. Though they could not see each other, chicks never emerged together, but the dominant moved forwards under cover while constantly uttering a typical note. This might have served as a signal to the subordinate who never called while emerging to feed.
Social Hierarchy and Weight Hierarchy Social hierarchy followed weight hierarchy so that from hatching to fledging, dominant young were heavier than their subordinate siblings. Weight differences ranged from 1% on the hatching day to 38% at day 5, but the percentage difference usually diminished towards fledging (Fig. lb). In three broods the social rank of individual young transposed during the course of their life, and in two cases a viral disease (Safriel and Harris, in preparation) was detected. In all three cases the weight rank was also transposed to correspond with the rank of the social hierarchy.
Hierarchy, Hatching Sequence and Initial Weight Among eight broods for which information was sufficient, six had a social hierarchy that followed the rank of weight at hatching and two had no differences in initial weights within broods (of two young each). The average interval between successive hatchings in 50 clutches (checking intervals of 1-12 h) was approx. 8 h (Safriel, in preparation). Thus, Oystercatchers hatch fairly synchronously, but the detectable intervals enable one to rank the chicks' hatching order. In most broods for which laying order, hatching order, and social rank were determined, peck order followed laying and/or hatching order: 71% of a young hatched from eggs laid first, and 75% of a young were first to hatch (Table 1). A multiple regression analysis suggests that 38% of the variance in the weight of the young at hatching (expressed as a proportion of mean weight of young in the brood) is attributable to the egg weight (expressed as proportion of mean weight of egg in its clutch), but that the contribution of hatching order is small (2%) and insignificant. However, 44% of the variance in hatching order of young is explained by the order of laying of the eggs from which they hatched, and an additional 22% by the proportional weight at which they hatched. Thus, the way egg material is distributed between successive eggs and the way the incubation regime during the laying period is patterned determine the offspring's social rank. First-hatched young are often already heavier at hatching, while late-hatched ones are usually much lighter. Social order may therefore depend on both hatching order and weight hierarchy, the latter being reinforced by the former.
Table 1. Social hierarchy related to laying and hatching sequences. Figures stand for number of young a Social rank
a
b
c
Laying sequence First Second Third
5 2 0
3 4 0
0 1 1
Hatching sequence First Second Third
6 2 0
3 4 1
0 I 1
a Cases of transposed social rank and of simultaneous hatching are omitted
Social Hierarchy and Fledging Success Of the four broods with no disease (two young in each), in two the a young alone fledged, and in two both siblings fledged. Of the six broods with disease and no transposition of rank, in only one did the a young not fledge, and in only one was there a b fledgling. Of the three broods in which social rank was transposed, all three young that acquired the a rank late in life fledged, and of the three young that acquired the b rank late in life, one did not fledge. The above observations combined (fledged/ notfledged: a 9/1; b 5/5) show the expected trend of very high fledging success only among dominant young. However, possibly due to the small number of cases, the difference in survival between the a and b young does not quite reach the level of 5% significance (p=0.065 Fisher exact one-tailed test). The major source of young mortality on Skokholm is predation by gulls (Safriel 1967). The only time a gull was observed attacking a young chick of known social rank, the chick was a subordinate. Indeed, subordinates sometimes stood exposed near their hiding, calling and rather restless.
Discussion
The pens were instrumental in elucidating the adaptive significance of the social hierarchy since they provided an experimental set-up in which the following attributes were achieved. First, food shortage was achieved. (Food around the pens was depleted and had to be transported along increasing distances. Failing to elicit the young's proper response to their luring attempts, the parents gradually lost the drive for full parental care.) Second, aggression among siblings was achieved. (Confinement to the small pen seemed responsible for the lack of suppression of overt aggression known among broods hand-reared
62 in captivity; Lind 1965) Third, predation was eliminated. (Gulls seemed suspicious of the pens and never preyed in them.) Thus, food shortage caused marked weight differences among siblings, and the careless behaviour of the underweight chicks increased their vulnerability. Because predators avoided the pens, these young would eventually have died of starvation instead, had they not been released. Carelessness, in the form of increased exposure and vocalization, also occcurred among unconfined subordinate young and could have contributed to their low survivorship. However, the events observed in the pens point to the advantage all siblings had of an established non-aggressive social hierarchy. Though always winning contests, the skirmishes would have also endangered the dominant siblings had they not been protected by the pens. On the other hand, replete, unconfined subordinates behaved 'properly' so that they had good chances of evading predation. The social hierarchy among Oystercatcher siblings is a brood-reduction adaptation, benefiting both parents and offspring. When food is in short supply, predators rapidly eliminate the subordinates (otherwise doomed to prolonged starvation), and food can then be given just to the few young the parents can amply support, thus guaranteeing a positive fledging success. When food is abundant, fledging success may increase because even subordinates can then minimize their exposure. Parents bring only one food item at a time, and the hierarchy prevents siblings from rushing together to the parent and fighting over the item; such behaviour may attract predators, and the young would then be taken even when not at the brink of starvation. Indeed, in spite of initial weight differences within some broods, all the siblings survived. With ample food, the light sibling was not hungry enough to behave carelessly, and the hierarchy saved chicks from pointless, but dangerous clashes. The interests of the subordinate young are also served. Giving way is advantageous provided that: (a) the increased chance of survival (if successful in securing an item in a fight) is outweighed by the increased chance of mortality (if engaged in a predator-attracting fight); (b) food supply does not vary erratically, i.e. if risking a fight over a food item at the time when food is short is disadvantageous, because the food situation is unlikely to improve in the future. Indeed, the cases in which unconfined subordinates did try to snatch food from dominants were among limpet-fed broods. On Skokholm, such broods are generally less well off than others (Safriel 1966), and due to unpredictable sea conditions, the supply of that food type may be erratic. Both the young and their parents are involved
in the maintenance of the mechanism for brood reduction: the parents by associating egg-weight hierarchy with laying (and hatching) order, and the young by non-aggressively accepting a social hierarchy founded on hatching priority and/or initial weight supremacy. On the other hand, in birds such as owls (e.g. Lack 1954) brood-reduction is exclusively controlled by parents through hatching asynchrony, which is much more pronounced than in the Oystercatcher. Most fully precocial birds are not fed by parents, and among them mechanisms for brood-reduction are not known. Even though fully precocial broods are hard to observe in nature, they have been studied in captivity; aggression, later transformed into stable social hierarchy, was noted in geese (Rades/iter 1974) and in tetraonids (Rajala 1962). The Oystercatcher falls into the category of birds with fully precocial young that are fed by parents. Among these, brood reduction is achieved through overt aggression (in cranes, Miller 1973), but through an accepted social hierarchy (in grebes, Fjeldsfi 1973; Simmons 1974). Avoidance of fighting among grebes is probably beneficial in preserving energy, whereas in the Oystercatcher, it provides an anti-predation measure. Brood-reduction in the Oystercatcher could have been more efficient if its hatching asynchrony were greater (e.g. 48 h as in the Crested Grebe Podiceps cristatus, Simmons 1974). Both the young and the nest of the Oystercatcher are more vulnerable to predation than those of the grebe, however. Long hatching intervals would have required feeding the young in the vicinity of a nest in which eggs were still being incubated, a precarious situation under predation pressure. Indeed, in most other Charadrii where young are not fed by parents, hatching is synchronous and the young leave the nest as soon as they dry. Their parents lure the first-hatched chicks back to the nest to await the completion of hatching, or they desert the late eggs (Ashkenazie and Safriel 1979). Feeding of the young in Oystercatchers is an adaptation associated with the specialized nature of their diet (Safriel 1967). Like many birds that feed their young and encounter difficulties in predicting food availability, the Oystercatcher has acquired a broodreduction mechanism. Rather than abandoning the 'traditional' hatching synchrony of the Charadrii, however, a neat social hierarchy among siblings has evolved.
Acknowledgements.During the courseof this study I greatlybenefited from the supervision and criticism of the late D. Lack. I also wish to thank C.M. Perrins, M.P. Harris, M. Norton-Griffiths, M. Cullen, J. Kear, and R. PrOs-Jones for support, discussions, and comments. I would also like to thank C.K. Britton, M. Alexander,and O. Safrielfor their help in the field.
63
References Ashkenazie S, Safriel UN (1979) Breeding cycle and behavior of the Semipalmated Sandpiper at Barrow, Alaska. Auk 96 : 56~67 Fjelds~ J (1973) Territory and the regulation of population density and recruitment in the horned grebe Podiceps auritus arcticus Boje, 1822. Vidensk Medd Dan Naturhist Foren 136 : 117-189 Lack D (1954) The natural regulation of animal numbers. Clarendon Press, Oxford Lind H (1965) Parental feeding in the Oystercatcher. Dan Ornithol Foren Tidsskr 59:1-31 Meyburg B-U (1974) Sibling aggression and mortality among nestling eagles. Ibis 116:224 228 Miller RS (1973) The brood size of cranes. Wilson Bull 85:436441
Procter DLC (1975) The problem of chick loss in the South Polar Skua Catharacta maccormicki. Ibis 117:452-459 Rades/iter T (1974) On the ontogeny of orienting movements in the triumph ceremony of two species of geese (Anser anser and Branta canadensis). Behaviour 50:1 15 Rajala P (1962) On the ecology of the broods of Capercaillie (Tetrao urogallus), Black Grouse (Lyrurus tetrix), and Willow Grouse (Lagopus lagopus). Suom Riista 15: 28 52 Safriel UN (1966) Food and survival of Oystercatcher chicks on Skokholm in 1965. Ibis 108:455 Safriel UN (1967) Population and food study of the Oystercatcher. PhD thesis, Oxford University Simmons KEL (1974) Adaptations in the reproductive biology of the Great Crested Grebe. Br Birds 67:413437
