Sibling competition and siblicide in asynchronously-hatching broods of the cattle egret Bubulcus ibis

Anita_ Behav., 1985, 33, 1228 1242

Sibling competition and siblicide in asynchronously-hatching broods of the cattle egret Bubulcus ibis MASAHIRO FUJIOKA

Laboratory of Animal Sociology, Faculty of Science, Osaka City University, Sugimoto, Sumiyoshi-ku, Osaka 558, Japan Abstract, Feeding behaviour and sibling competition were observed in nine families of the cattle egret

(Bubulcus ibis) from blinds during 1359 nest-h throughout the nestling period. During days 0-19, size differences among siblings were clear; begging behaviour of chicks changed with time. At least one parent always attended the nest. Food boluses regurgitated early within a feeding period were received by senior chicks more often than by juniors. When any two siblings begged for food at the same time, the elder and younger received the first bolus on 65% and 35% of occasions respectively. Between days 20 and 39, the frequency of begging reached a peak. Begging behaviour became intense and stereotyped. The number of boluses received per begging declined rapidly, especially for junior chicks. In large broods, the success rate of begging was lower and fights occurred among siblings, especially among juniors. Out of 256 dyadic fights, the elder sibling won 85, lost one, and tied 171. The youngest chick died in two broods, apparently as the result of these fights (siblicide). No parents interfered in fights among their offspring. After day 40, the frequency of begging decreased gradually and ceased by day 80, No chicks died in the last period, although the frequency of fights in all large broods remained high.

Parents of many birds create size asymmetries among their offspring through asynchronous hatching (see Clark & Wilson 1981 for a review), or through variation in egg-size (e.g. Parsons 1970, 1975; Howe 1976, 1978). Various hypotheses have been proposed for the significance of asynchronous hatching. For birds in which food requirements of chicks show a marked peak, it may be favourable for parents to shift the peak (Hussell 1972; Bryant 1978): this is the 'peak load reduction' hypothesis. Asynchronous hatching has been more generally regarded, however, as a mechanism by which brood size can be adjusted to food availability during the nestling period (Lack 1947, 1954; Ricklefs 1965; O'Connor 1978a): this is the 'brood reduction' hypothesis. Delayed growth and low survival rates of weaker or smaller chicks have been reported for many asynchronously hatching birds (see Howe 1976; O'Connor 1978a; Hahn 1981 for reviews). Two mechanisms of brood reduction have been distinguished by Braun & Hunt (1983): the starvation of weaker chicks unable to compete for food and aggressive activities between siblings that result in the weaker chick either being denied access to required resources or being killed (see also Mock 1984a). The latter process should rather be termed 'siblicide' (first used by Gould 1982) rather than 'fratricide', as used by O'Connor (1978a),

when the victim's sex is unknown or unspecified (Mock 1984a). In many asynchronously hatching birds, brood reduction occurs through passive starvation (e.g. Ricklefs 1965; Howe 1976). Inoue (1981, in press) has shown that weaker little egret chicks (Egretta garzetta) are not favoured when two siblings beg for food because of the change in feeding procedure from 'indirect' to 'direct' methods (see also Mock 1985). The idea that nestling growth rates may be maximal as an evolved response to such sibling competition (O'Connor 1978b; Werschkul & Jackson 1979) is presumably applicable also to such behavioural developments. On the other hand, siblicide has been reported in many raptors and some other birds (see O'Connor 1978a; Stinson 1979; Mock 1984a for reviews). However, interactions between parents and offspring and among siblings, in relation to food delivery, which are involved in mechanisms of brood reduction, have rarely been directly observed in birds. On the other hand, several authors have pointed out that, theoretically, there may be parent-offspring conflict over brood reduction (Hamilton 1964; Alexander 1974; Trivers 1974; Macnair & Parker 1979). O'Connor (1978a) modelled hypothetical thresholds of brood reduction for the parents, survivors and victim, and concluded that

1228

Fujioka: Sibling competition in cattle egrets brood reduction might be a strategy preferred by survivors even at the expense of the parent's reproductive success. Alexander (1974) and Hahn (1981), however, regarded brood reduction as a parental manipulation in order to maximize parental inclusive fitness. This problem of who wins the conflict in the course of the evolution of brood reduction mechanisms remains unsolved. In the cattle egret (Bubulcus ibis), it takes 6.3 +2-8 SD days on average for an entire brood to hatch (range 1-16 days) (Fujioka 1984). Here I report on observations of parent-offspring interactions and sibling competition in nine egret families throughout the nestling period (50-80 days), with some theoretical considerations of the significance of asynchronous hatching and of parent-offspring conflict. The aims of this paper are to clarify (1) the mechanisms of brood reduction in the cattle egret and (2) the proximate factors of brood reduction.

METHODS The study was conducted in a mixed,species heronry in Mie Prefecture, Japan (34~ 136~ The colony has been established for many years on a small island (50 x 300 m) in a lake (see Fujioka & Yamagishi 1981 for a more detailed description). More than 500 pairs of four egret species nest in the trees: cattle egrets, great egrets (Casmerodius aIbus), little egrets and intermediate egrets (Egretta intermedio), plus many black-crowned night-herons (Nycticorax nycticorax). Two blinds were constructed at the top of scaffold towers (3'3 and 3'6 m high) in the colony, to allow close-range observation of the nests 3-10 m away. I observed each of nine focal families approximately every 5 days. A total of 848.8 h of direct observation was made over 70 days from 8 June to 10 September 1978. Fewer than six nests (generally one or two), within the range of observation, were observed simultaneously with the unaided eye or with binoculars (9x35). Day-time observation usually began just after sunrise and continued until about 30 min after sunset. I recorded the presence of parents and chicks, all occasions when feeding took place, and interactions among siblings during 1359 nest-h (115 nest-days). Adult birds were identified by differences in or idiosyncrasies of external morphology. Parental sexes could not be determined except for pair D in which copulations were observed. Downy nestlings

1229

were individually marked with coloured felt-tip pens and, after they reached about 10 days old, by ringing their legs. Parent cattle egrets feed their chicks by regurgitating food boluses. A 'feeding series' consisted of a series of regurgitations and/or two types of parental behaviour inducing chicks to beg (described below). For the purpose of analysis, two such incidents were considered to belong to the same feeding series if they occurred within 5 rain of each other. The relative lengths of food boluses were estimated by comparison with the parent's bill length (circa 5-6 cm). Chicks showed several types of begging behaviour (see Fig. 2) and parents showed two types of behaviour inducing chicks to beg: (1) pointing their bill at the chicks and (2) regurgitating a bolus to the tip of their bill and then swallowing it. For each regurgitation or begging-inducing behaviour, each instance of begging behaviour by the chicks was recorded. Begging behaviour by the chicks was also recorded just before and just after each feeding series. A chick occasionally showed two types of begging behaviour at one regurgitation or begginginducing behaviour; in this case, each type was recorded as 0.5 instances of that behaviour. Whenever a food bolus was received by more than one chick, it was assumed to have been equally divided between them: for the sake of convenience in the analysis, the amount received by each chick was recorded as the reciprocal of the number of recipients. As an index to satisfaction in receiving food, the 'Success Rate' for each chick was calculated from the number of food boluses received as a percentage of the number of begging incidents by the chick. When any two siblings begged at the same time, the percentage of cases where one obtained food prior to the other was termed the 'Priority Ratio' of the former (called the 'success ratio' in Inoue 1981, in press). Two types of fights among siblings were distinguished, as follows. In 'Weak Pecking', two siblings faced each other at close range, with necks fully extended and exchanged weak blows without injuries. In 'Serious Fights', one chick pecked, pulled, thrust down, and/or jumped on another sibling which then counter-attacked, escaped, or fell from the nest. A Fight Bout consisted of a series of blows between siblings; two blows were considered to be part of the same Fight Bout if they occurred within 1 rain of each other. Fights

Animal Behaviour, 33, 4

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Figure 1. The number of nest visits with food (solid line) and parental attendance (broken line). Vertical lines represent _+lSD. Parental attendance is the percentage of periods during which at least one parent of a pair stayed on the nest or within 5 m of the nest. Data from trio X are excluded.

between three or more siblings were analysed further by dividing them into dyadic fights 9 Losers in W e a k Pecking crouched; in Serious Fights they escaped or fell from the nest. Cases where a loser could not be determined were regarded as ties. Nest, pairs, b r o o d s a n d families are represented by capital letters (e.g. nest Q), a n d chicks by lower-case letters in alphabetical order of h a t c h i n g (a, b . . . . ). The age of chicks was counted in days after h a t c h i n g (hatching day =zero). F o r analysis of the d e v e l o p m e n t of a n d changes in b e h a v i o u r of chicks a n d parents, the nestling period o f each nest was divided into 10-day stages based on the age of the a-chick; day 0 (hatching day of a) to day 9 is called stage I, day 10 to day 19 is stage II, a n d so on. Stage VII included all days after day 60. Average b r o o d size was 3.4 chicks per nest. Hereafter b r o o d s of four a n d five chicks are called 'large' broods; these do n o t include b r o o d D because its a-chick was lost to p r e d a t i o n before its d-chick hatched. Three adults attended nest X, p r e s u m a b l y consisting of one male a n d two females.

RESULTS

Attendance and Visits Both parents c o n t r i b u t e d to b r o o d i n g a n d guarding the chicks almost equally. D u r i n g stages I

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Figure 2. The change in begging behaviour in relation to the chicks' real age. The data were combined from 31 chicks of nine broods. Numbers of sample chick-days are shown above the figure. Begging behaviour of each type was defined as follows, in increasing order of intensity. AP type (N=224): a chick attempts to peck or grasp the parent's bill but cannot reach it. P type (N=632.5): a chick softly pecks any part of the parent's bill. G type (N=499.5): a chick lightly grasps the parent's bill. GP type ( N - 1024.5): a chick firmly grasps the parent's bill crosswise near the base and pulls the parent's head down to the level of the nest. In AGP type (N=2613.5), the chick attempts to grasp and pull the parent's bill with its own neck and legs fully stretched, but does not reach the parent's bill because it is held up high. H type (N=61): a chick harasses and pursues the parent with AGP type of begging, while the parent walks or flies to avoid the violent begging.

Fujioka: Sibling competition in cattle egrets and II, if either parent left the nest to forage, the other brooded or stood nearby to guard the chicks, so parental attendance was nearly 100%. In contrast, after stage III, both parents spent little time in the vicinity of the nest (Fig. 1). At stage III, parental attendance varied widely between nests, ranging from 70' 1% for nest V to 11 '7% for nest W. The parents of large broods stayed for shorter periods than those of broods with three chicks, though the difference was not significant: 19"1% versus 45.3% (Mann-Whitney U-test, U-=2). The number of nest visits with food increased gradually until stage III then decreased later (Fig. i). The maximum number of daily visits in each brood was not greatly different between large broods (mean = 7.3) and small broods (mean = 6-1; Mann-Whitney U-test, U = 3'5, ys).

1231

time particularly in stages 1-III (Fig. 2). Begging frequency peaked at stage IV and decreased rapidly thereafter (Fig. 3). After about day 40, seniors began to forage by themselves near the heronry. The nestling period could be divided into three phases on the basis of the type and frequency of begging behaviour. During the 'early phase' (stages I-II), begging behaviour changed rapidly with higher-intensity types becoming more frequent as time went on. Thereafter, it became highly stereotyped and reached a peak frequency (the 'middle phase', stages III-IV). The 'late phase' (stages V VII) was characterized by a rapid decline in begging frequency.

Feeding During a total of 115 nest-days, 780 feeding series were recorded in the nine broods. A feeding series lasted from less than 1 min up to 17 min, with a mean of 3.2 rain. Out of a total of 2569 boluses regurgitated, 87 were not eaten by chicks and nine were snatched by chicks of neighbouring nests. Seizing a bolus that had already been received by a sibling was observed seven times. Any remains of

Begging Young cattle egrets begged their parents for food in the nest or, during later stages, near the nest (see Fig. 2). They did not pursue their parents more than about 10 m from the nest even when they were able to fly well. Begging behaviour changed with

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1232

Animal Behaviour, 33, 4

food boluses on a nest were reconsumed by the parent. In addition, focal chicks were seen to snatch seven food boluses from an adult other than their parents. Parents regurgitated an average of 3.29 food boluses per feeding series (range= 1-11, N=780 feeding series), and the average number of feeding series per nest visit was 1.74 (range= 1-9, N=447 visits). Each parent regurgitated an average of 11.8 boluses per day ( r a n g e - I 34, N=217 parentdays). The average length of food boluses was 0.8 times the parent's bill length with a maximum of 2.0 times (N= 1194 boluses). The length of food boluses did not seem to change as the chicks grew, although most estimations were made during the early stages (I-II) of the nestling period (many food boluses could not be seen adequately during later stages due to direct feeding methods: see below). Two types of feeding were distinguishable. In 'indirect feeding,' a parent regurgitated a food bolus onto the nest-floor, and the chicks pecked the bolus; frequently most of it remained uneaten. In 'direct feeding', a parent transferred a food bolus directly to a chick that had grabbed the parent's bill crosswise. In cases of the latter type of feeding, generally only one chick received a food bolus at once, although other siblings sometimes picked up a scrap that had been dropped accidentally by the first receiver. Out of 770 boluses fed by indirect feeding, 292 (37.9%) were eaten by one chick and the others were shared by siblings . In contrast, 1276 out of 1421 boluses (89"9%) fed by direct feeding were monopolized. This difference is highly significant O( 2 = 660"4, df = 1, P < 0001). Frequency of feeding appeared to reach a peak much earlier than that of begging (Fig. 3). However, the real mass of food eaten by chicks was overestimated in indirect feeding because chicks often left some of the food bolus and the parent then reconsumed the remainder. Reconsurning behaviour by parents was observed frequently during stage I, but decreased rapidly thereafter (Fig. 3). Thus the real mass of food supplied by parents or received by chicks was estimated to be at a maximum during the middle phase. In addition, the two types of parental display inducing chicks to beg were restricted to the early stages. The frequencies of displays where a parent pointed its bill at the chicks and where a parent regurgitated a bolus to its bill tip then swallowed were respectively as follows: 8-2+_9-2 SD and 5.8_+9.2 so at stage I;

9.2_+8-5 SD and 6.6+_7.9 SD at stage lI; 1"1 +2"2 SD and 1.6 + 3"8 SD at stage lII; and fewer than 1'6 for both displays after stage IlI.

Food Contests

Figure 4 shows the change in Success Rate with time. The Success Rates of a-, b- and c-chicks were clearly higher than those of d- and e-chicks during stages II-V, especially at stage III. Success Rates overall declined during stages l l l V . By stage VII, most chicks were already independent, so little begging was recorded during this stage. Success Rate was smaller for large broods than for small broods (Mann-Whitney U-test, U=7, P < 0.002; Table I). It is noteworthy that Success Rates were low for broods S and V, the parents of which ($2, V1 and V2) had underdeveloped plumage. Table I also shows an apparent tendency for elder chicks to have higher Success Rates compared with younger siblings in each brood: Success Rate corresponded to hatching order in 17 dyads of consecutively-hatched siblings and was reversed in only five such dyads (Z2=6.55, df= 1, P<0.02). The Success Rates of b-chicks in broods U and R were especially high because they were both reared for a long period after all their siblings had died or become independent.

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Fujioka: Sibling competition in cattle egrets

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Figure 5. The number of boluses received by chicks (black bars) in relation to the sequence of regurgitation within a feeding series. Expected values (white bars) were calculated by allocating food boluses to the observed chicks in proportion to their observation time, assuming no differencein competitiveability or food demand among siblings.The only e-chick died in stage IV, so no data were obtained for it after this stage. The number of boluses received by chicks was analysed with respect to the sequence of regurgitations within a feeding series (Fig. 5). During stages I-If, a- and b-chicks received more food boluses than expected from regurgitations early in the series (the first to the third), while c- and dchicks received fewer than expected. The proportion of food boluses received by c- and d-chicks increased for regurgitations late in the series. The difference between observed and expected values decreased somewhat during stages II[-IV. During stages V-VII, food boluses were allocated equally among all chicks. The Priority Ratio was always greater than 50~ for the elder chick in all dyads, with one exception, The difference in Priority Ratios within a dyad was smaller between consecutively-hatched chicks than between those separated by several siblings (Table II, Z2=7.30, dr=l, P<0.01). The total Priority Ratio of elder chicks tended to be slightly larger during the early phase than during the later phases: 64.9~ at stages I-II (N= 285), 60.2% at stages III-

Table 1I. Priority Ratios in relation to difference in hatching order within sibling dyads Priority Ratio (%) Difference in hatching order 1-2 3M

Elder Younger 59.2 71.2

40.8 28.8

Total no. 887 139

IV (N= 563), and 56.2~o at stages V-VII (N= 178), with an overall mean of 60.8% (N= 1026). Mean overall Priority Ratios of each chick declined with hatching order: a = 6 0 . 7 ~ (N=550), b=54.7~o (N= 572), c = 44.0% (N= 545), d = 36.7~ (N= 305), and e = 33.3% (N= 78).

Fights and Siblicide There were 91 Fight Bouts between two chicks

Fujioka." Sibling competition in cattle egrets

1235

Table lII. Winning and losing in fights* among siblings Winner Loser

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* Figures refer to total no. of fights (Serious Fights + Weak Pecking) with no. Weak Pecking given in parentheses. ~ Fights won was calculated from total no. of fights. All ties (171 Serious Fights and 21 Weak Pecking) are excluded.

and 44 among three chicks or more (one chick attacked two or more or vice versa, or a number of chicks attacked each other); the latter cases were converted into 192 dyadic fights for further analysis. Fight Bouts generally ended within 1 min, though they occasionally lasted for several minutes ( m a x i m u m = i n t e r m i t t e n t Weak Pecking for 14 min). Weak Pecking rarely occurred after stage I. The age of the oldest chick to show Weak Pecking was 11 days. Weak Pecking was mutual in 23 (85.2~) of 27 dyadic fights and one-sided in the other four (14.8~). The winner and loser were clear in only six cases (22.2~; Table III). Weak Pecking was not associated closely with feeding; only eight Fight Bouts (29.6~) occurred during a feeding series or within 1 min before or after. Almost all Serious Fights occurred after stage II (see Fig. 8 for examples), and occurred only during feeding or within 1 min before or after feeding, with three exceptions (one case occurred when chicks in a brood begged from an adult not their parent). In 85 (33.2~) of 256 Serious Fights, the attack was one-sided or the identity of the winner was clear; the losing sibling was excluded fi-om food contests, at least temporarily. All losers except one were younger than the winner (Table III). In the other 171 Serious Fights, the fighters tied, i.e. they pecked each other and stopped fighting before the winner was decided. Younger siblings did not initiate fights against older ones. Parents did not interfere either in Weak Pecking or in Serious Fights among their offspring.

Weak Pecking was observed in all broods except brood V. Serious Fights occurred more frequently in large broods (0"96/dyad/day, N = 118) than in small broods (0.27/dyad/day, N = 2 1 9 ) , although this was not statistically significant (t = 2.01, df= 6, P < 0.1). The frequency of fights in a brood tended to be inversely proportional to the average Success Rate in the brood (Fig. 6). Serious Fights were observed in dyads of all possible hatching orders, but most Serious Fights occurred between d- and e-chicks. Junior chicks

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1236

Animal Behaviour, 33, 4

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fought more frequently than senior chicks (Fig. 7), meaning that most losers were d- and e-chicks, i.e. the youngest chicks in large broods. In two large broods, the youngest sibling died, apparently as a direct or indirect result of fights with its siblings (siblicide); d in brood W died between days 24 and 28 and e in brood X died between days 32 and 35. Figure 8 shows the frequency of fights in three large broods. The frequency of fights in broods W and X first reached a peak just before the siblicide and then quickly declined. About 10 days after the brood reductions, fighting resumed and was mostly directed at the youngest siblings remaining in each brood. In contrast, fighting rates became high only once (at about day 40) in brood T. In nest W, parent W1 visited the nest only half as often as parent W2 during stage III, when the youngest chick died. As the d-chick in brood W was still young, it was probably killed easily by a small number of fights (see Fig. 5 in Fujioka 1984 for the growth of brood W). On day 26 in nest X, the dchick (aged 23 days) violently and repeatedly pecked e (aged 22 days) until the latter escaped from the nest. The d-chick even disregarded feeding in the process (two instances). Though the e-chick was not attacked much just before its death (aged 27 days), it mostly stayed under the nest, avoiding attacks by siblings, and begged less often than its elder siblings in spite of appearing hungry. In nest T, the d-chick grew more slowly than its elder siblings (see Fig. 5 in Fujioka 1984), but survived and became independent. Out of 71 Serious Fights in brood T, 32 in W and 118 in X, 50-7%, 56"3%, and 62.7% respectively were directed at or exchanged with the youngest sibling (after the youngest died the next youngest sibling was considered as the 'youngest sibling'). There was a clear

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Figure 8. The number of fights in three large broods. Shaded parts represent fights in which it was possible to determine the winner and loser. Broken linesrepresent the number of Weak Pecking bouts. The youngest chick in broods W and X presumably died of siblicide about the time shown by the arrows.

loser more frequently in broods W (46.8%) and X (65.2%) than in brood T (4.2%). Overall, the youngest sibling lost fights and was excluded from contests for food much more frequently in broods W (34'4%) and X (46'6%) than in brood Y (4'2%). Although siblicide was not observed directly in this study, it was observed in 1982 in the same study area (Fujioka 1985).

DISCUSSION

Two Aspects of Sibling Competition There are two aspects of sibling competition in the cattle egret: food contests and direct fights. These two aspects correspond with (passive) starvation and siblicide in the process of brood reduction, as recognized by Braun & Hunt (1983) and Mock (1984a). In general, siblicidal death is a result both of injuries or falling to the ground due to direct attack, and of starvation through aggressive exclusion from feeding (Braun & Hunt 1983; Mock 1984a). Three phases of the nestling period are recognizable on the bases of these aspects of sibling competition (Table IV).

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Animal Behaviour, 33, 4

Large differences in body size among siblings are produced by hatching asynchrony that spans an average of 6"3 days in this study population (Fujioka 1984). These size differences are maintained or increased during the early phase because chicks grow rapidly until about 20 days old (Fujioka 1984). Such rapid growth has been considered as a strategy of chicks to out-compete siblings for food or parental care (O'Connor 1978b; Werschkul & Jackson 1979). Competition for food may have resulted in selection for rapid development of chick begging behaviour, as well as rapid chick growth. The rapid changes in size and begging behaviour (Fig. 2) and, as a result, in feeding methods, ensure that junior chicks stand little chance of obtaining food until senior siblings have received several boluses (Figs 4, 5). Similar behavioural transitions have been described quantitatively in the little egret (Inoue 1981, in press), two ardeidae species (Mock 1984b) and the black legged kittiwake, Rissa tridactyla (Braun & Hunt 1983), and have been outlined in the cattle egret (Blaker 1969), other herons (Meanley 1955; Owen 1955; Werschkul 1979; Rodgers 1980), and three passerine species (Bengtsson & Ryd6n 1981). In the year of my study, two out of nine chicks starved at stage I in 29 nests that were not observed directly (Fujioka 1984). Size differences among siblings become small later because the sigmoid growth curve flattens out after day 20 (Fig. 4 in Fujioka 1984). Begging behaviour becomes stereotyped (Fig. 2) and its frequency reaches a peak during the middle phase (Fig. 3). As previously described by many authors (e.g. Kluyver 1950, cited in Bengtsson & Ryd6n 1981; Perrins 1965; Bengtsson & Ryd6n 1981), begging is more frequent when chicks are insufficiently fed. Thus cattle egret chicks are likely to be hungriest during the middle phase (Fig. 3), although, during this period, parents are visiting the nest with food most frequently (Fig. 1). Suddenly, in this phase, Serious Fights begin to occur, especially in large broods (Fig. 8). The elder participant usually wins or ties in a Serious Fight (Table III), thereby excluding younger siblings from food contests for a while and occasionally injuring them. No siblicide occurs during the late phase. Potentially lethal aggressive interactions may be induced when the rate of food delivery decreases abruptly, e.g. during a severe storm, because Serious Fights still continue to be frequent (Fig. 8). However, by

this stage, even the weaker chicks are more difficult to kill, and are able to move about enough to become 'scavengers'. Some large egret chicks were observed living as scavengers in the heronry. Proximate Factors of Brood Reduction

Recently, Mock (1984b, 1985) clearly demonstrated that food size (i.e. whether or not one chick can monopolize the food) is an important proximate factor of sibling aggression. Food boluses regurgitated by cattle egret parents contain some insects (mainly Orthoptera), plus frogs, etc., tightly bound together by mucus. Boluses cannot be swallowed whole by small cattle egret chicks but can be monopolized by large ones. This may be one of the reasons why Serious Fights occurred after the early phase. However, compared with cattle egret chicks, little egret chicks are much less aggressive, yet they also receive food of monopolizable size (Inoue, in press, personal observations). It is likely that an insufficient delivery rate of food is an important proximate factor in brood reduction. The frequency of fighting in a brood was inversely proportional to the average Success Rate in the brood (Fig. 6). Starvation occurred only in large broods (Fujioka 1984) and siblicide occurred in two large broods in which the Success Rate was low (Table I), and during the middle phase (stages III-IV) when the conditions of food availability were most severe for all chicks (Fig. 4). For a while after a case of siblicide occurred, there were few fights in the broods concerned (Fig. 8), suggesting that food conditions for surviving chicks became better. In diurnal raptors and owls the adaptive significance of siblicide has not been clearly explained (Brown et al. 1977; Stinson 1979). Some authors have contended that inter-sibling strife takes place in the presence of abundant food and is entirely unaffected by the availability of food (e.g. Ingram 1959; Meyburg 1974), but quantitative data are lacking. In ospreys (Pandion haliaetus), sibling aggression, whereby elder siblings gain more food, occurs only in colonies or nests where food is limited (Poole 1982). Sensitivity to the amount of food available may differ between 'obligate' siblicidal species and 'facultative' ones (Edwards & Collopy 1983; Mock 1984a). Aggressiveness of captive sandhill crane chicks (Grus canadensis) increases when there is food stress (Quale 1976), but no similar tendency is found in great egret chicks (Mock, personal communication).

Fujioka: Sibling competition in cattle egrets" The Success Rate was low in brood T (Table I), but all the chicks became independent. Serious Fights occurred frequently in the brood, but most (96%) of them were tied (Fig. 8). The growth of the d-chick in brood T was rather slow for the first few days (Fig. 5 in Fujioka 1984) and its Success Rate was also conspicuously lower than those of its elder siblings (Table I). These facts suggest that asymmetry in competitive ability among siblings may reduce aggressive interactions among them (the 'sibling rivalry reducing hypothesis': Hahn 1981). In other words, if competitive ability differs enough among siblings, the senior siblings may not need to attack the weakest sibling because they will be able to obtain food prior to the weakest chick without fighting. This benefits the older chicks because (1) proximately, they can reduce the energy used in fights and (2) ultimately, their inclusive fitness will be higher if the weakest sibling can survive (assuming they obtain enough food for themselves). In support of this interpretation, it is notable that siblicide occurred early in brood W (Fig. 8), where the Success Rate was actually higher for the d-chick than the c-chick (Table I). Additionally, in an experiment, even-aged chicks fought more often than asynchronously-hatching chicks (Fujioka 1985). Meyburg (1974) has shown that, in some eagles, the younger chick is subject to attack by the elder if the hatching interval is short, but that the younger quickly dies of starvation and the elder's attacks on it are unimportant if the hatching interval is long (see also Hahn 1981). In summary, the primary proximate factor in brood reduction is probably an insufficient rate of food delivery to the brood. When competitive ability differs substantially among siblings, starvation may occur more easily at an early stage of the nestling period and the occurrence of siblicide may be reduced later. Relative food size for chicks may influence the mechanisms of brood reduction, starvation or siblicide, but not the timing of brood reduction.

Significance of Asynchronous Hatching Four hypotheses have been proposed for explaining the significance of asynchronous hatching. The 'insurance hypothesis' is usually applied to species such as pelicans, cranes, terns, and raptors, which are characterized by small clutches and long nestling periods (see Stinson 1979 for critical discussion). Females start full incubation with the

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first egg and, according to this hypothesis, lay the second egg mainly to insure against infertility of the first. Should both hatch, the younger tends to die quickly as a result of starvation and/or siblicide (e.g. Meyburg 1974; Nisbet & Cohen 1975). However, both chicks are reared in about 20% of cases in the golden eagle, Aquila chrysaetos (Brown & Amadon 1969). In addition, this hypothesis cannot fully explain the existence of many birds that lay only one egg in a clutch. Hussell (1972) has proposed that reduction of the time between laying the first egg and fledging the first chick might be an important factor selecting for asynchronous hatching in arctic passerines, in response to the effects of adverse weather and predation. Recently, this idea has been expanded as the 'nest-failure hypothesis' by Clark & Wilson (1981). However, selection to reduce predation will be stronger for behaviour that shortens the nestling period rather than the incubation period because predation rates are generally higher during the nestling period. A sibling hierarchy can also result from differences in chick size due to variation in egg-size rather than asynchronous hatching. This strategy may be adopted under intense predation because it is not accompanied by elongation of the nestling period, whereas asynchronous hatching is. Sibling hierarchies resulting from egg-size variation are known in several bird species (Parsons 1970, 1975; Howe 1976, 1978; Bryant 1978; O'Connor 1978b; Ricklefs et al. 1978). The third hypothesis was also proposed by Hussell (1972): the peak load reduction hypothesis. For bii'ds in which the food requirements of chicks show a marked peak, as in the house martin, Delichon urbica (Bryant 1978), it will be advantageous for parents to spread the peaks of individual chicks, even over a few days. The begging frequency of cattle egret chicks showed a sharp peak in the middle phase (Fig. 3) and both instances of siblicide in this study occurred during this period (Fig. 8). Therefore, differences among siblings in their stage of growth will be advantageous, at least to parents. A higher, sharper peak of begging frequency in experimental even-aged broods than in asynchronously-hatching broods (Fujioka 1985) also supports this hypothesis. Asynchronous hatching has been explained primarily as a mechanism for brood reduction in a habitat with unpredictable food resources: the brood reduction hypothesis (Lack 1947, 1954; O'Connor 1978a). In many bird species, brood

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reduction and/or delayed growth of junior chicks occurs as a result of insufficient food in asynchronously-hatching broods (see Howe 1976; O'Connor 1978a; Hahn 1981 for reviews). This provides some support for the brood reduction hypothesis. Most phenomena observed in this study can be regarded as mechanisms for brood reduction, avoiding total loss of the brood and thus wasteful investment when food resources are scarce. This explanation is compatible with the peak load reduction hypothesis and the sibling rivalry reducing hypothesis discussed above.

Parent-offspring Conflict According to the concept of inclusive fitness (Hamilton 1964), all members of a family will conflict to some degree over the timing of brood reduction (Alexander 1974; Trivers 1974; O'Connor 1978a; Mock 1984a), that is they will benefit by the death of their kin at different degrees of food deficiency. The brood reduction hypothesis cannot predict whether brood reduction will occur through sibling competition, parental manipulation or suicide. There is little evidence that parents do not favour weaker/smaller chicks when food is scarce. On the other hand, many reports, including this study, have demonstrated that brood reduction generally occurs with the death of weaker/ smaller chicks as a result of sibling competition. The parents apparently do not interfere in sibling competition for food, or even in lethal aggression, although parental brooding may suppress sibling aggression at least temporarily (Meyburg 1974; Cooper 1980). Spellerberg (1971) reported that, in MacCormick's skuas (Catharaeta maccormicki), parents intervened between fighting siblings, but finally the a-chick succeeded in killing the b-chick (see Mock 1984a for other examples of parental suppression). Why do cattle egret parents not interfere in competition among their offspring? Their feeding capacity seems to exceed demand by chicks during the early stage of the nestling period (Figs 1, 3, 4), as has been shown in several bird species (Kluyver 1961; Perrins & Moss 1975). Therefore parents could avoid starvation of their offspring by delivering more food or by favouring younger offspring. In spite of this, the initial size differences among chicks remains or increases, sometimes to the extent that the weakest chick starves (cattle egret: Blaker 1969; Siegfried 1972; Fujioka 1984; other

birds: e.g. Ricklefs 1965; Balph 1975; O'Connor 1975). However, it should be emphasized that the number of chicks that parents can raise will be decided by food availability at the 'bottle-neck', i.e. at the time of peak food requirements by the chicks (O'Connor 1978b). During the middle phase, food is relatively insufficient (Fig. 4) and most of the time parents arc away from the nest foraging (Fig. 1). Even if parents interfere in sibling competition during feeding, elder siblings can kill while the parents are absent. If the parents attempt to interfere further, they may have to decrease their foraging time. Thus, parents are unable to interfere in sibling competition in their broods. In addition, it should be noted that extra-pair copulations are common in the cattle egret, especially after the middle of the egg-laying period (Fujioka & Yamagishi 1981). Polygynous trios with one nest (e.g. nest X) occurred occasionally in the study population. These conditions could facilitate the evolution of aggressive interactions among siblings and indifference of parents toward sibling competition, because the coefficient of relatedness among family members may be less than 0.5 (Macnair & Parker 1979).

Concluding Remarks Asynchronous hatching in cattle egrets could have evolved as an adaptation to their unpredictable food resources, mainly grasshoppers and other insects in open habitats. Asynchronous hatching produces a clear size hierarchy among siblings, by which brood reduction through starvation can easily occur if the rate of food delivery is insufficient. Parents can manipulate hatching intervals and control their investment. However, when the food demands of chicks reach a sharp peak, parents face the alternatives of delivering more food or intervening in competition among their offspring, and they select the former. Therefore, starvation and siblicide may occur at higher rates than is optimal for parents (but this may be undetectable in the face of ecological uncertainties: Mock, personal communication). Such selfish behaviour of siblings could evolve because the advantages of the behaviour to the perpetrator exceed the future disadvantages of the same behaviour by its own offspring. The reduction of the peak load of food delivery and of wasteful sibling rivalry will also be advantageous to egrets.

Fujioka: Sibling competition in cattle egrets' ACKNOWLEDGMENTS I would like to t h a n k Satoshi Yamagishi for his encouragement, advice a n d criticism t h r o u g h o u t this study. Special t h a n k s to Douglas M o c k for his m a n y c o m m e n t s on the m a n u s c r i p t a n d for prepublication copies of various papers. David Werschkul, Yoshiaki ItS, Keisuke Ueda, Y u k i h i k o K o j i m a a n d Michiko I n o u e also offered useful c o m m e n t s o n the manuscript. Yukio Higuchi, Y o s h i k a z u Inoue, a n d Shigemoto K o m e d a assisted with field work. Hiroyoshi Higuchi, Takeshi Shiota, Y o u k o Y a m a g u c h i , Y o s h i t o O h s a k o a n d S. K o m e d a helped with o b t a i n i n g literature. I t h a n k t h e m all. This work was supported in p a r t by a G r a n t - i n - A i d for Special Project Research on Biological Aspects o f Optimal Strategy a n d Social Structure from the J a p a n Ministry of Education, Science a n d Culture.

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(Received 2 May 1984; revised 21 August 1984; MS. number: 2534)