Sibling Aggression, Hatching Asynchrony, and Nestling Mortality in the Black Kite (Milvus Migrans)

Behav Ecol Sociobiol (1999) 45: 33±45 Ó Springer-Verlag 1999

ORIGINAL ARTICLE

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

Received: 9 March 1998 / Accepted after revision: 8 August 1998

Abstract In siblicidal species, hatching asynchrony high-quality chicks, but a manifestation of a parent- could act to reduce sibling rivalry or promote the death ospring con¯ict over brood size. of last-hatched chicks. The pattern of hatching asynchrony was experimentally altered in the black kite Key words Hatching asynchrony á Sibling aggression á Milvus migrans. Hatching asynchrony in control broods Nestling mortality á Parent-ospring con¯ict á was intermediate between those of experimentally syn- Milvus migrans chronised and asynchronised broods. Sibling aggression and wounds on the chicks were more commonly observed early in the nestling period and in synchronous nests. Serious injuries were observed on last-hatched Introduction chicks in asynchronous nests, as were observations of intimidated or crushed chicks. Sibling aggression was Sibling aggression and hatching asynchrony are com- related to food abundance, but some chicks died at an mon in raptors (Newton 1979), and may promote sib- early age in nests with abundant food (cainism). Cainism licide (Simmons 1988). Hatching asynchrony could was more commonly found in asynchronous nests. For reduce sibling aggression between size-matched chicks species with facultative siblicide, moderate hatching (Hahn 1981), allowing the establishment of a size hier- asynchrony could be a compromise between reducing archy with a minimum of aggressive interactions. Al- sibling rivalry and avoiding large size dierences be- ternatively, it could promote the death of last-hatched tween sibs that would result in cainism. Female black chicks by establishing large size dierences between kites preferentially fed the smallest chicks and exhibited siblings, since in obligately siblicidal species (those in behaviours to reduce sibling aggression, contrary to which >90% of last-hatched chicks die; Simmons 1988), observations in other siblicidal species. In a highly op- hatching asynchrony is higher than in facultative species portunistic forager such as the black kite, a strategy may (those in which siblicide occurs in <90% of nests; exist to protract the life of all the chicks in the brood, Meyburg 1974; Edwards and Collopy 1983; Anderson waiting for unpredictable situations of food overabun- 1989). These two hypotheses are not mutually exclusive, dance. This would induce the appearance of a parent- and there may exist an optimal intermediate degree of ospring con¯ict over brood reduction, re¯ected in the hatching asynchrony (Mock et al. 1990; Osorno and existence of a possible anticipated response by some of Drummond 1995). The research in Ardeidae, Phalacro- the chicks (cainism) and in the appearance of special coracidae and Sulidae indicates that synchronisation of behaviours by the parents to selectively feed smaller hatching in siblicidal species may escalate the combats chicks or reduce sibling aggression. In this facultatively (Fujioka 1985a; Mock and Ploger 1987; Anderson 1989; siblicidal species, cainism does not seem to be the ®nal Osorno and Drummond 1995), while highly asynchro- stage of an evolutionary trend favouring the raising of nous hatching may result in poor growth of last-hatched chicks, excluded from food transfer by their larger siblings (Amundsen and Stokland 1988; Mock et al. 1990; see also Pinajowski 1992). This possible ``cost'' of J. VinÄ uela (&) hatching asynchrony on growth of last-hatched chicks Departamento de EcologõÂ a Evolutiva may exist even in Passerines, where sibling aggression is Museo Nacional de Ciencias Naturales, (C.S.I.C.) JoseÂ Gutierrez Abascal 2, E-28006 Madrid, Spain negligible or absent (see Slagsvold et al. 1995). e-mail: [email protected], Siblicide may contribute to food-dependent brood Tel.: +34-1-4111328, Fax: +34-1-564078 reduction if sibling aggression is causally linked to 34 hunger (Lack 1954). Thus, hatching asynchrony would Large size and good condition at ¯edging may be promote the establishment of a size hierarchy (VinÄ uela important factors to assure prebreeding survival and 1996), and sibling aggression would facilitate brood re- future breeding in species with high prebreeding mor- duction when there is no food available to raise all tality and strong competition for nesting territories. chicks. However, experimental evidence suggests that Furthermore, the retention of the second egg may al- much of the mortality induced by hatching asynchrony low parents to track population conditions (Simmons is not adaptive (Amundsen and Slagsvold 1991), but a 1988, 1993): raising only one high-quality chick when negative consequence of an early onset in incubation, population density is high (when territorial competi- which would be favoured for other reasons (review in tion is high), raising two lower-quality chicks when Stoleson and Beissinger 1995). Furthermore, in obligate population density is low. Simmons (1988) proposed siblicidal species, there is no relationship between food several predictions of his hypothesis that could be abundance and sibling aggression (Simmons 1988; tested in long-lived facultatively siblicidal raptors. Gargett 1990; Mock et al. 1990), and it is not clear to Speci®cally, the frequency of appearance of siblicide or what degree sibling aggression is related to food abun- the variation in the factors promoting it (hatching dance in facultatively siblicidal species (Mock et al. asynchrony, long laying intervals, intraclutch egg size 1990; Forbes 1991a). variation) should be correlated with population densi- Sibling aggression could be unrelated to food abun- ties. dance if there is a parent-ospring con¯ict over brood The black kite, Milvus migrans, is a medium-sized, reduction (O'Connor 1978; Parker and Mock 1987; relatively long lived raptor (a maximum of 22 years in Anderson 1990a; Nilsson 1995; RodrõÂ guez-GironeÂ s the wild; Newton 1979), exhibiting facultative siblicide 1996). Ospring may tend to commit siblicide under less and cannibalism (Jones and ManÄ ez 1990; VinÄ uela 1991). stringent conditions than those optimal for parents, so Black kites are highly opportunistic predators, obtaining selection would favour the appearance of behavioural their food by a searching strategy, and their broods are patterns allowing parental regulation of siblicide (An- exposed to very variable provisioning rates depending derson 1995). Theoretical models predict that parent- on environmental conditions (see e.g. VinÄ uela and Veiga ospring con¯ict over brood size should be more prev- 1992). This study addresses the following questions. (1) alent among species exposed to highly variable provi- Can hatching asynchrony reduce sibling rivalry? (2) sioning rates (Forbes 1991b, 1993; Forbes and Ydenberg Does hatching asynchrony promote the death of last- 1992; RodrõÂ guez-GironeÂ s 1996). However, there is little hatched chicks? (3) Is sibling aggression related to food empirical evidence for such con¯ict (Drummond et al. availability? (4) Is there any evidence suggesting the 1986). Parent raptors do not seem to interfere in sibling existence of a parent-ospring con¯ict over brood re- ®ghts or exhibit any behaviour regulating the brood duction in a species with highly variable provisioning reduction process (Newton 1979; Forbes 1991a; but see rates? (5) Is there any eect of brood size or nestling Gerrard and Bortolotti 1988), but most information has mortality on the ¯edging size or condition at ¯edging of been gathered in obligate siblicidal species (Meyburg dominant chicks? Furthermore, I test some of the pre- 1974; Gargett 1990). Little is known about the mecha- dictions of Simmons (1988) in a steadily increasing nisms, if any, allowing parental regulation of sibling population of a facultatively siblicidal raptor, in which competition (Simmons 1988; Anderson 1995). the breeders were exposed to very dierent population There has been much discussion about the signi®cance densities during a 3-year period. of obligate siblicide, typical of some species laying two eggs (Stinson 1979; Simmons 1988, 1991; Mock et al. 1990; Gargett 1991). The second egg may be an ``insurance'' in case the ®rst egg does not hatch (Meyburg 1974; Stinson 1979; Parker and Mock 1987; Anderson 1990b; Methods Mock et al. 1990). However, evidence supporting the ``insurance value'' of last-laid eggs is scant (but see Forbes The study was conducted in Matas Gordas, Northern DonÄ ana et al. 1997). This prompted Simmons (1988) to propose an National Park (south-west Spain, 37°N6°5¢W). This is an open and alternative: obligate siblicide would be the consequence of ¯at area of Mediterranean forest (cork oaks Quercus suber), scrublands and grasslands, close to a seasonally ¯ooded marshland an evolutionary trend favouring the raising of high- (see VinÄ uela and Veiga 1992). quality chicks. Chicks raised in the absence of a compet- The breeding area was visited almost daily (>95% of days) itive sibling would reach a higher size or better condition from the start (mid-March) to the end (end of July) of the breeding at ¯edging than senior chicks competing with siblings for seasons of 1987, 1988 and 1989. Nests were visited daily during laying and eggs were marked with felt pens. Laying was considered food, all else being equal (Stinson 1979; Simmons 1988), to be ®nished when the third egg was found or if 4 days elapsed but few data are available to support this idea. Simmons' since the previous one was found. After laying, nests were not hypothesis is intimately related to recent work supporting visited again until 28±30 days after the date of laying of the ®rst the hypothesis that hatching asynchrony in Passerines can egg. Nests were visited daily during hatching, and the chicks indi- be a mechanism to ensure the rearing of high-quality vidually marked under the wing with felt pens. Brood size at hatching varied between one and three chicks. Nests in which only ospring (Slagsvold et al. 1995; Amundsen and Slagsvold one chick hatched have not been considered, unless otherwise in- 1996, 1998). dicated in the text. 35

Hatching asynchrony two chicks died, the average of ages of death for each sibling was considered. During 1988 and 1989, hatching asynchrony of 52 randomly selected clutches was experimentally altered by removing the eggs as they were laid and replacing them with hen eggs arti®cially marked Sibling aggression to mimic the natural pigmentation of kite eggs. From these nests, the ®rst two eggs were taken on the days they were found, and were During 1988 and 1989, aggressive behaviour between siblings just held until 3 days after the second egg was laid, when they were after arriving at the nests was recorded. These attacks were pecks returned to the nest. Third-laid eggs were marked when found, but given mostly on the head, especially around the beak and eyes, and not removed. Experimental clutches were alternatively assigned to on the nape. During these ®ghts, the chicks also apparently tried to one of two treatments: (1) asynchronous clutches had eggs main- twist the neck of their opponent by grasping its head or neck and tained during the removal period in incubators at 37±38 °C, with shaking it strongly from side to side. When aggression was ob- water containers below the eggs (Campbell and Flood 1977; served, the number of pecks given by the chicks during the ®rst Burnham 1978, 1983), and (2) synchronous clutches were not in- minute after the start of the ®ght was recorded. The number of cubated, but maintained at ambient temperature during the re- pecks given by all chicks in a brood during each visit have been moval period. Eggs in both treatments were turned 180° twice pooled. Young chicks (0±10 days old) have no well-developed daily. Hereafter, experimental nests are named asynchronous and recognition abilities, and they often begged the observer for food synchronous, while nests with unaltered hatching asynchrony are (see Delannoy and Cruz 1988 and Gargett 1990 for similar obser- named controls. vations in other raptors). Sibling aggression in raptors occurs es- Hatching asynchrony was de®ned as the time elapsed in hours pecially when the female is absent from the nest (Newton 1979). between hatching of ®rst and last eggs in the clutch, and was esti- These absences must be rare during the early nestling period, since mated following a variation of the method of Stokland and brooding in black kites is almost continuous during the ®rst Amundsen (1988) (VinÄ uela 1996). For the analyses of variation in 2 weeks after hatching (Cramp 1980; Koga and Shiraishi 1987; hatching asynchrony in control nests among years, only the cases in personal observation). Thus, nestling behaviour during early nest which the ®rst- and last-laid eggs in a clutch hatched have been checks, just after the female was ¯ushed from the nests, may be a included. For all analyses, hatching order has been considered in- good estimate of the level of aggression. Between 10±20 days of stead of laying order (in most of the synchronous nests hatching age, the chicks changed their behaviour, remaining crouched down, order was opposite to laying order; VinÄ uela 1997a). adopting defensive attitudes, or even attacking the intruder, but Hatching asynchrony of control nests was intermediate between rarely fought each other (see below). Those cases in which the older those of experimental synchronous and asynchronous nests (Ta- sib in a brood was lying on a smaller sibling, or the smallest chick ble 1; VinÄ uela 1996). was clearly intimidated on the nest rim (head lowered and body tightly crouched down, as observed in the ``loser'' chicks after a Nestling mortality ®ght) were also recorded. The occurrence of wounds on the chicks was also noted on All nests were visited 2±3 days after hatching of last chicks, and every nest check. Only recent wounds and those partially scarred, every 4±7 days (mostly every 5 days) thereafter until the end of the but not recorded during the previous visit, were considered. I nestling period. On each nest check after hatching, I renewed the counted the total number of wounds found on all the chicks in a marks on the chicks and recorded cases of mortality. In some cases brood and at every nest check. In the most extreme cases, the back of predation, clues from the predator were found (mainly tawny of the injured chick was plucked and bloody (see Meyburg 1974), owls Strix aluco), and in all of them the complete brood was or the eyes were so seriously wounded, the chick could no longer depredated. Total brood losses in raptors are usually related to open them. A score of 12 wounds was assigned to these large in- predation (Newton 1979). All nests in which there was nestling juries (one more that the maximum number of discrete wounds mortality due to other causes (predation, abandonment and nest found per chick during the whole study). collapse) have been excluded from the analyses of nestling mor- The nestling period was divided into nine periods (Fig. 1), de- tality by starvation or siblicide. However, three cases in which the pending on the age of the older chick in the brood. When more broods were depredated near the end of the nestling period, well than one visit was made in one of these age periods, averages for all beyond the maximum age of death by starvation or siblicide re- the visits within each time period were calculated. To analyse the corded during the 3 study years, have been considered as nests eect of brood size on sibling aggression, the averages of attacks/ without starvation or siblicide mortality. Black kite chicks have a wounds for ®rst- and second-hatched chicks and attacks/wounds high resistance to food deprivation, often suering important for third-hatched chicks were calculated (Table 2). growth delays due to protracted periods of food scarcity (Hiraldo To avoid pseudoreplication, averages of each variable for each et al. 1990; Veiga and Hiraldo 1990). This facilitated the detection nest were used in all the analyses, except those relating behaviour of this kind of mortality, as the chicks suered evident retarded and age of the chicks. For the analyses involving the variables growth and were extremely emaciated before death. ``mean number of attacks'' and ``mean number of wounds'', non- Age of death for every chick was estimated assuming that death parametric statistics were used, because inspection of plots and occurred half way between the day on which the death was detected preliminary analyses on transformed and untransformed variables and the previous visit. For the three broods with three chicks where did not provide evidence of normality. During every nest check, prey remains at the nest were recorded (see VinÄ uela and Veiga 1992 for details). Black kites have very poorly developed nest-cleaning habits, and most prey remains are Table 1 Hatching asynchrony (h) in black kite broods of two and not removed from the nests, so they may provide a reasonable three chicks. Variation between control nests (natural hatching estimate of food provisioning for comparative purposes (VinÄ uela patterns) and experimental nests (hatching synchronised or asyn- 1991). On every nest check, prey remains without meat were re- chronised by altering incubation pattern during the laying period). moved, and those that could still be eaten marked, to avoid re- Sample sizes in parentheses peating records in subsequent visits. Biomass of prey was estimated from values reported in the bibliography and from my own ®eld Clutch size Treatment measurements of fresh and entire prey (VinÄ uela 1991). To estimate Asynchronous Control Synchronous biomass of rabbits, the main prey in this area, tarsus of rabbit remains were measured, and biomass estimated following Delibes Two eggs 82.4 33.1 (11) 53.9 23.8 (35) 19.8 14.9 (9) and GarcõÂ a (1984). Total estimated biomass recorded at every nest Three eggs 108.7 13.7 (4) 89.7 20.9 (23) 34.5 21.4 (4) check was divided by the number of days elapsed since the previous visit to obtain a rate biomass/day that could be compared among 36

dierent nests. For the analyses of rate of attacks among chicks younger than 10 days (see below), the daily prey biomass during the same period in which the aggressive behaviour was recorded for each nest was considered. Aggressive behaviour of nestlings and the behaviour of chicks and adults during feeding bouts was observed in two nests during June 1988 using a spotting scope at a distance of 150±200 m, and at four nests during May and June 1989 from blinds on towers at a distance of 100±150 m from the nest trees. Observations were made during early morning and late evening, probably the birds' most active time, and behaviour was recorded on tapes. Before the observations, chicks were individually marked on the head with felt pens.

Test of Simmons' hypothesis

Following Simmons (1988), I de®ned cainism as siblicide in the absence of food shortage. To explore the possible eects of brood size or brood reduction on the quality of senior chicks, ¯edging size was recorded, and an estimate of condition for all the chicks surviving to ¯edging age has been used. Fledging mass and tarsus length at ¯edging were considered to have been reached when the seventh primary was 180 mm long (VinÄ uela and Veiga 1992). The residuals of the regression of ¯edging mass on (tarsus length)3 was used as an estimate of condition at ¯edging. The population of black kites in my study area increased more than twofold from 1987 to 1989, mainly due to the arrival of new inexperienced pairs (details in VinÄ uela 1993, 1997b). In the last study year, one of the highest population densities recorded for this species was reached (VinÄ uela et al. 1994). In subsequent years, the numbers in the study area have remained stable (F. Hiraldo, personal communication), so the population in 1989 can be considered saturated. The frequency of appearance of cainism was compared between years (i.e. between dierent conditions of population density) and brood sizes. For some analyses, I distinguished between pairs in their 1st or 2nd breeding year in a nesting territory (inexperienced birds), and those with 3 or more years of settlement in the area (experienced birds) (details in VinÄ uela 1993, 1997b). The laying interval between ®rst and second eggs was not accurately known, since the nests were not visited daily before laying, but the number of days elapsed between laying of second and third eggs in three-egg clutches was accurately recorded. To estimate the relative size of last-laid eggs, I have used an index similar to that Fig. 1 Variation during the nestling period of mean number of proposed by Slagsvold et al. (1984), but I considered the relative wounds found on the chicks (a) and mean number of attacks size of last-laid eggs with respect to the largest egg in the clutch, observed during nest checks (b). Values are means S.E. for every instead of the average mass of the clutch (see VinÄ uela 1997b). This age period (referred to the age of the older chick in the brood). index was mass of last-laid egg ´ 100/mass of largest egg (the ®rst Number of nest visits above bars in most two-egg clutches and the second in most three-egg clutches; VinÄ uela 1997b).

Table 2 Attacks and wounds observed in broods of two chicks, Results between ®rst- and second-hatched chicks of three-chick broods, and those involving third-hatched chicks. Averages are for each brood during nestling period (Wounds) or for chicks younger than Chick mortality by starvation and siblicide 10 days (Attacks). Number of broods and means SD for each category. Averages with dierent superscripts are signi®cantly dif- The productivity of two- and three-egg clutches, de- ferent (Mann-Whitney U-tests, P < 0.05) pending on the treatment, is shown in Table 3. Five chicks Two chicks Three chicks were found dead in the nest with wounds in the head or the back, of which three also had their neck apparently 1st±2nd 3rd twisted. In two asynchronous nests, last-hatched chicks with a full crop were found dead below their much larger All nests 44 18 Attacks 1.1 2.8ab 1.5 2.9a 0.2 0.5b siblings. In these cases, the small chick was probably Wounds 1.3 1.7 1.2 1.5 1.1 1.6 crushed or asphyxiated, another kind of siblicide, as Control nests 26 12 previously suggested for other species of raptors (Wend- ab a b Attacks 0.2 0.5 0.6 1.5 0 land 1958 in Meyburg 1974). In eight broods, the smallest Wounds 1.2 1.7 0.7 0.6 0.7 1.2 chick was observed intimidated on the nest rim. Four of 37

Table 3 Mean SD number of chicks ¯edged in broods of the 1989, cainism occurred more frequently in asynchronous black kite during 1988 and 1989 (sample size in parentheses) with (4 cases in 14 nests) than in control nests (2 cases in 34 variation in original clutch sizes (one-egg clutches excluded) and treatment. Only broods where more than one chick hatched are nests) (Fisher exact test, P 0.04), but there was no shown. Broods where chicks were lost due to causes other than dierence between control and synchronous nests (no brood reduction (predation, abandonment or nest collapse) were cases in 11 nests). excluded

Clutch size Treatment Number of ¯edglings Age at death Two eggs Asynchronous 1.5 0.5 (4) Control 1.5 0.5 (19) Most of the chicks died from starvation or siblicide at a Synchronous 1.7 0.5 (6) young age (27% of deaths aected chicks younger than 5 Three eggs Asynchronous 1.6 0.5 (8) days; Fig. 2). A multifactorial ANOVA revealed signi- Control 2.1 0.6 (17) Synchronous 2.2 0.7 (6) ®cant and independent eects of year, brood size and treatment on the age at death (log-transformed) (F5,32 4.5, P 0.003). Age at death was lower in these chicks were found dead or dying on the ground be- 1987 (6.1 11 days, n 7) than in 1988 low the nests 24±72 h later. Similar cases have been de- (12.2 8.2 days, n 16) or 1989 (14.1 9 days, scribed for other raptor species and are considered n 15) (partial F2,32 7.2, P 0.003), because another form of siblicide (Meyburg 1974). cainism was more frequently observed during 1987 (see The existence of siblicide was also con®rmed by direct below), and chicks lost due to cainism died at a younger observations. I witnessed the older chick of a two-chick age than chicks lost to starvation (F1,36 23.4, brood pecking its sibling for 4 h in the evening, after P < 0.001; Fig. 2). Chicks in control broods tended to 12 h without food. The next morning the smaller chick die at an older age (13.4 10.1 days, n 18) than appeared partially eaten in the nest. Five chicks younger chicks in asynchronous (8.9 6.5 days, n 10) or than 5 days disappeared from nests, and have also been synchronous broods (8.6 8.6 days, n 3) (partial considered as cases of siblicide, because they were partial F2,32 3.2, P 0.055). Age at death was lower in losses unrelated to abandonment or nest collapse, and three-chick (8.2 7.8 days, n 18) than in two-chick predation caused complete loss of the brood, as ob- broods (15.1 9.5 days) (partial F1,32 5.2, served in other raptors (Newton 1979). P 0.03). In 29 of the 31 chicks which died from starvation, signs of aggression were also recorded (direct observations or wounds on the chicks). Also, in 6 out of the 17 Sibling aggression and hatching asynchrony cases assigned to siblicide, the dead chicks had starvation symptoms. Thus, both kinds of mortality were The variables used to estimate the levels of sibling ag- clearly associated, as observed in other raptor species gression did not signi®cantly vary from 1988 to 1989 (Newton 1979). However, in the remaining 11 cases of (Mann-Whitney U-tests of averages for each brood; siblicide, the chicks died without having showed signs of sibling aggression: Z 0.97, P 0.33; wounds: starvation or retarded growth, at an early age (Fig. 2), Z 0.8, P 0.42; `crushing': Z 1.33, P 0.18; and in nests where food was plentiful (estimated daily `nest rim': Z 1.2, P 0.14), so data from both years biomass in the nests from hatching of the ®rst chick to have been pooled for subsequent analyses. the day on which the death was discovered: The chicks exhibited aggressive behaviour towards 223 183 g, range: 50±673). These cases are considered their siblings as early as the day of hatching. Sibling cainism, following Simmons (1988). During 1988 and aggression was observed more frequently among younger chicks (Kruskal-Wallis ranks test, H 30.8, P < 0.001, Fig. 1). For subsequent analyses, I consider the mean number of attacks for chicks 0±10 days old, when they still did not show any fear or defence reaction against the observer, and when most of the aggressive interactions were recorded. The mean number of attacks was higher in synchronous than in control (Z 3.5, P < 0.001) or asynchronous nests (Z 2.1, P 0.03), but there were no signi®cant dierences between asynchronous and control nests (Z 0.36, P 0.71) (Fig. 3). In three-chick broods, ®ghts between ®rst and second chicks were more commonly observed than attacks on third-hatched chicks (Table 2). There was no signi®cant dierence in the rate of attacks Fig. 2 Frequency distribution of the age at death by starvation between two- and three-chick broods, even when con- (hatched bars) or siblicide (white bars) sidering only control nests (Table 2). 38

number of wounds did not signi®cantly vary with brood size or between hatching orders in three-chick broods, even when considering only control nests (Table 2), or only the average for chicks younger than 10 days.

Sibling aggression, prey biomass and nestling mortality

As expected in this highly opportunistic species, the average daily biomass found in the nests was very variable (208 117 g/day; range: 30±535). The same was Fig. 3 Mean + SE number of attacks (white bars) and wounds true when considering only the ®rst 10 days of the nes- (hatched bars) observed during nest checks in control (n 38), experimentally synchronised (n 12) and synchronised (n 12) tling period (203 131 g/day; range: 7±633). The av- broods. Averages for every brood during the nestling period erage daily biomass in nests where starvation mortality occurred was signi®cantly lower than in nests without mortality or nests with cainism. Biomass was similar for The mean number of observations of last-hatched no-mortality and cainistic nests (Table 5). Biomass was chicks below their larger siblings was higher in asyn- higher in three-chick (250 125 g/day) than in two- chronous broods, although signi®cant dierences were chick (191 111 g/day) broods (two-way ANOVA, found only when comparing asynchronous and syn- mortality: F2,56 5.9, P 0.005; brood size: F1,56 chronous broods (Z 2.09, P 0.037, Table 4). The 6.8, P 0.011). Average daily biomass was not signif- mean number of observations of chicks intimidated on icantly aected by the year (1988: 186.5 110 g/day; the nest rim tended to be higher in asynchronous than in 1989: 223 121 g/day; F1,60 1,4, P 0.23) or control (Z 1.9, P 0.055) or synchronous broods treatment (asynchronous broods: 194.5 108 g/day; (Z 2.13, P 0.033) (Table 4). Brood size did not control broods: 215 115 g/day; synchronous broods: signi®cantly aect either of these two variables (crush- 200 139 g/day; F2,59 0.17, P 0.84). ing: Z 0.04, P 0.96; nest rim: Z 1.3, P Mean prey biomass was negatively correlated with 0.19). average number of attacks on chicks younger than The mean number of wounds per visit increased to a 10 days (rs )0.25, P 0.051, n 62). No correla- maximum when the older chick was 15±19 days old and tion was found between prey biomass and mean number declined thereafter (Kruskal-Wallis, H 39.4, of wounds (rs )0.15, P 0.23, n 62) for all nests P < 0.001, Fig. 1). The average number of wounds was pooled, but when considering only the nests with mor- higher in synchronous than in control nests (Z 2.13, tality from starvation, this correlation was signi®cant P 0.03), but not higher than in asynchronous nests (rs )0.43, P 0.027, n 26). (Z 1.1, P 0.27) (Fig. 3). Asynchronous nests also Broods that lost some chicks by cainism or starvation had a relatively high mean number of wounds, but the had higher rates of wounding than broods without dierence with control nests was not signi®cant mortality (Table 5) but, although the nests with cainism (Z 0.17, P 0.86). This probably re¯ects a high showed high rates of aggression (Table 5), no signi®cant variance in the mean number of wounds found in dierences were found for this variable. asynchronous nests (Fig. 3). Most serious injuries (to which the highest score was assigned) were found in asynchronous nests (a chick between the sticks of the Quality of senior chicks nest rim with a dislocated leg, and three chicks with large plucked and blooded areas on the back and head). Final size and condition of senior chicks were highly However, wounds were rarely seen in other asynchro- variable, as might be expected in a species with a highly nous nests, probably due to early intimidation of last- hatched siblings in nests where food was abundant and, Table 5 Mean daily biomass, estimated from prey remains found consequently, chick aggressiveness was low. The mean in the nests, mean number of attacks among chicks younger than 10 days, and mean number of wounds on chicks in broods without mortality and in nests with mortality by starvation or cainism. Table 4 Mean (SD) number of observations of oldest chicks Averages for each brood type during the nestling period. Data lying down on their smaller sibling (Crushing), and smallest chicks pooled for 1988 and 1989. Means with dierent superscripts are intimidated on the nest rim (Nest rim) in control and experimen- signi®cantly dierent (ANOVA and post-hoc Tukey HSD test for tally synchronised or asynchronised broods. Averages for each biomass, and Mann-Whitney U-tests for attacks and wounds) brood during the nestling period No mortality Starvation Cainism Crushing Nest rim (n 29) (n 26) (n 5)

Asynchronous (n 12) 0.11 0.21 0.10 0.17 Biomass (g) 246 117a 165 98b 246 152a Control (n 38) 0.04 0.08 0.02 0.07 Attacks 1.4 3.2 0.9 2.5 3.1 4.5 Synchronous (n 12) 0 0 Wounds 1 1.2a 1.9 2.1b 2.5 1.8b 39

¯exible growth (Hiraldo et al. 1990; VinÄ uela and Veiga 1992; Table 6). Tarsus length was not signi®cantly af- fected by any of the variables considered (year, brood size, mortality or treatment; Table 6). Fledging mass and condition of senior chicks were signi®cantly aected by year, brood size and mortality, but not by treatment (Table 6). Fledging size or condition did not dier between senior cainistic chicks or senior chicks in broods without mortality (Table 6). However, senior chicks in broods where chicks died from starvation had lower ¯edging weight and worse condition than senior chicks in broods without mortality (Table 6). Fledging mass and condition of senior chicks were lower in 1989 than in 1987 or 1988 (Table 6), as previously reported in a subsample of this population (VinÄ uela and Veiga 1992). Senior chicks in broods where only one chick survived had lower mass and poorer condition than senior chicks in multiple broods (Table 6). Considering simultaneously all the variables in multifactorial ANOVAs, I 3 found signi®cant eects of year (F 5.5, P Fig. 4 Condition at ¯edging (mass/tarsus length ) of senior chicks 2,70 of black kites related to the study year and occurrence of nestling 0.006) and brood size (F2,70 14.4, P < 0.001) on mortality (white bars no mortality, hatched bars starvation ¯edging mass, but not of mortality or treatment. The mortality, black bars cainism). Groups with dierent letters above same analysis with ¯edgling condition as dependent bars are signi®cantly dierent (ANOVA and Tukey HSD post-hoc test). Sample sizes are also given above bars variable revealed signi®cant eects of year (F2,66 8.5, P 0.001), brood size (F2,66 14.8, P < 0.001), and of the interaction year ´ mortality (F4,66 6.7, P < 0.001; Fig. 4). During 1988, senior chicks had a Test of Simmons' hypothesis similar condition in broods with or without mortality. In contrast, senior chicks in broods where a chick had Cainism occurred more frequently in three-chick (23% starved were in poorer condition than those in broods of 31 nests) than in two-chick broods (7% of 56 nests) without mortality during 1987 and 1989 (Fig. 4). (G 4.1, P < 0.05). Furthermore, cainism decreased from 1987 to 1989 (1987: 5 cases in 19 multiple broods, 26.3%; 1988: 4 cases in 26 nests, 15.4%, and 1989: 2 cases in 42 nests, 4.8%; G 8.3, P < 0.05), so cainism was less commonly observed as the population approached saturation and in small broods. Table 6 Fledging mass, tarsus length and ¯edgling condition [re- The laying interval between second and third eggs siduals of the regression of Fledging weight on (tarsus length)3]of senior chicks of black kites in broods where more than one egg varied between 2 and 4 days, and in most cases was hatched. Variation among years, mortality [0 broods without 3 days (71%) (mean SD 3.1 0.5, n 46). The mortality, 1 broods where a chick was lost due to starvation, 2 laying interval did not show any signi®cant variation broods where cainism (death of young chicks not associated with among years (F 0.9, P 0.4), and the relative food scarcity) occurred], ®nal brood size, and treatment (A ex- 2,45 perimental asynchronous nests, C control nests, S experimental size of last laid eggs did not vary signi®cantly among synchronous nests). Means SD. Means with dierent super- years (F2,124 0.06, P 0.94). Clutch size decreased scripts are signi®cantly dierent (ANOVAs and Tukey HSD post- from 1987 (2.8 0.4, n 21) to 1988 (2.4 0.6, hoc test, P < 0.05). Sample sizes are given in parentheses n 50) and 1989 (2.2 0.5, n 67) (F2,135 9.4, Variable Mass Tarsus Condition P < 0.001). This could be due to the increase in inexperienced birds among breeders from 1987 to 1989 (Vi- Year 1987 (17) 736 77a 57.2 1.6 11.7 66.3ab nÄ uela 1993), since inexperienced black kite pairs had 1988 (24) 737 62a 56.9 1.9 18 54.1a smaller clutches (experienced: 2.6 0.5, n 69; inex- b b 1989 (35) 694 85 57.1 1.7 )28.5 83.1 perienced: 2.2 0.5, n 69; F 22.7, P < 0.001). Mortality 0 (39) 747 64a 57.3 1.9 20.8 55.3a 1 (26) 670 89b 56.7 1.8 )44.8 88.7b However, a two-way ANOVA revealed independent ef- ab ab 2(10) 725 44 57.0 1.0 3.9 54.2 fects of breeder experience (F1,132 11.6, P < 0.001) Brood size 1 (24) 661 87a 56.9 1.3 )56.7 88a and year (F 10.6, P < 0.001). b b 2,132 2 (40) 739 63 57.1 2 16.3 53.9 Hatching asynchrony of control nests decreased from 3 (12) 755 46b 57.3 1.6 28.8 44.5b Treatment A (12) 713 107 57.6 1.3 )18 108.4 1987 (85.6 21.2 h, n 13) to 1988 (78.6 29.9 h, C (53) 709 75 56.9 1.9 )10.6 68.2 n 11) and 1989 (57.2 28.9 h, n 23) (F 5.2, S (11) 759 53 57 1.5 37.8 38.1 P < 0.01), but this may be a consequence of the inter- Total (76) Mean 717 79 57.1 1.7 )4.8 73.4 annual variation in clutch size, since hatching asynchrony Range 415±888 52±62 )312±128 in this species increases with clutch size (Table 1). A two- 40 way ANOVA of hatching asynchrony on clutch size and the largest chicks ®lled their crop, but the small one year revealed a clear eect of clutch size (F 22.5, obtained little food. After these feeding bouts, the fe- P < 0.001), but not of year (F 1.1, P 0.34). male brooded the chicks, but rising every 4±15 min, for periods lasting 3±4 min., and feeding two to six food morsels to the smallest chick, until the older chicks woke Observations of behaviour of parents and chicks up, when the female resuming brooding again. The female repeated this behaviour as many as four times after Sibling aggression was not recorded in a three-chick a ``normal'' feeding bout. brood observed for 26 h when the chicks were 25± During a feeding bout in a three-chick brood, when 40 days old. In contrast, in the ®ve nests observed when the two ®rst-hatched chicks were ®ghting strongly, the the chicks were 4±10 days old (two two-chick broods female pecked the head of the second-hatched chick, and and three three-chick broods), ®ghts between siblings placed herself between the two siblings before resuming were observed frequently, whenever the female was out feeding. of the nest or simply stood up on it. There were very marked dierences in the duration and development of ®ghts depending on the degree of hatching asynchrony. The longest (up to 15 min) and strongest ®ghts (two Discussion chicks with the head blooded after the ®ght) were observed between the ®rst and second chick of two three- Sibling aggression, age and hatching asynchrony chick broods (estimated hatching asynchronies of 31 and 7 h). In contrast, in a two-chick asynchronous brood Sibling aggression and wounds were frequently observed (estimated hatching asynchrony 85 h.) the ®ghts were in young chicks, but rarely in old ones. The reduction in brief, as the largest chick intimidated its sibling after one the frequency of observations of ®ghts could be due to to three pecks. the change in behaviour of the chicks towards the ob- Aggressive behaviour of chicks during feeding bouts server (see Methods). This change in behaviour could was also remarkably dierent depending on hatching also explain why the number of wounds reached a peak asynchrony and brood size. In three-chick broods later in the nestling period than the number of attacks (n 3), the two largest chicks (®rst and second hat- (Fig. 1). However, the frequency of observation of ched) tried to exclude the third-hatched sibling from wounds con®rms a reduction in aggressiveness during feeding, as they pecked it on the head whenever it tried the second half of the nestling period. This reduction in to rise, as happened in the two-chick asynchronous aggression as chicks grow older is the rule in birds brood. In contrast, the ®rst- and second-hatched chicks (Gargett 1970; Meyburg 1974; Mock 1984; Bortolotti of three-chick broods usually did not ®ght during feed- 1986a; Drummond and GarcõÂ a Chavelas 1989). Early in ing bouts, but tried to be the ®rst to get the food morsels the nestling period, the expected bene®ts (in terms of from the beak of the female, or they tried to snatch the food provisioning) for a siblicidal senior chick are food from their sibling's beak. However, in almost all greater than in later stages, so a higher level of aggres- the feeding bouts observed (31 out of 39), the female was sion would be expected among younger chicks (Forbes able to give some food to the smallest chick, even during and Ydenberg 1992). two feeding bouts 24±48 h before the last-hatched chicks Sibling aggression was more frequently observed in died in two nests. Two behaviours of the females that synchronous nests, as predicted by theory (longer/ resulted in the smallest nestling receiving some food stronger ®ghts among size-matched opponents; May- were recorded. nard Smith and Parker 1976). This result supports the The female usually entered the nest on the same side hypothesis that hatching asynchrony may act to reduce (usually the outer side of the crown of the tree), and the sibling rivalry (Hamilton 1964; Hahn 1981), as shown in chicks tried to stay as near as possible to that side, studies with herons (Fujioka 1985a,b; Mock and Ploger struggling to get the favoured position (``jockeying'' 1987), boobies (Anderson 1989; Osorno and Drummond behaviours, see Bengtsson and RydeÂ n 1983 and Gott- 1995), ospreys (Forbes 1991a) and American kestrels lander 1987). In three-chick broods, the two largest (Wiebe and Bortolotti 1994). In three-chick broods, siblings always monopolised the favourable position, sibling aggression between ®rst and second chicks was leaving the smallest chick at the back. During three more frequently observed than aggressions involving feeding bouts, the female, after giving some food to the third-hatched chicks. Similar arguments may be used in largest chicks, took the prey in her beak and walked this case, because hatching asynchrony between ®rst and around the nest rim until near the smallest chick and fed second chicks was smaller that that between second and it until the largest chicks again took the ``®rst-line'' third chicks, at least in control nests (VinÄ uela 1997a, position ahead of the small sibling. unpublished data). On four occasions I observed the female exclusively Given that hatching asynchrony did not clearly aect feed the smallest chick of one three-chick brood and the the size or condition of senior chicks (Table 6), it seems second-hatched chick of the asynchronous two-chick that the cost of enhanced sibling rivalry in synchronous brood. This occurred after feeding bouts during which nests is mainly re¯ected in the earlier age at death in 41 cases of brood reduction, in a slower growth of chicks in rabbits in years of high incidence of myxomatosis, dying synchronous broods, and in a small size of last-hatched ®sh or cray®sh when marshes dry out, or sporadic chicks in synchronous nests (VinÄ uela 1991, unpublished overabundance of rubbish from human activity; VinÄ uela data). Even in synchronous nests, a size hierarchy could 1991; VinÄ uela and Veiga 1992). Additionally, the ag- be noted in most cases (VinÄ uela 1996), so synchronisa- gressiveness of chicks could be unrelated to food abun- tion of hatching would simply delay the establishment of dance if they exhibit an anticipated response (see below), the hierarchy at a higher energy cost (slower growth) for and in fact, prey biomass at nests with cainism was not the ®nally dominant chick (Osorno and Drummond dierent from that in nests without mortality. A rein- 1995), or induce earlier mortality/poor growth. forcement of the aggressiveness of chicks by food scar- Cases of intimidation of the youngest chick and of city has been reported in several studies (Ingram 1962; the large chick lying on its younger sibling were more Procter 1975; Newton 1977; Poole 1979, 1982; Braun frequently observed in asynchronous nests. When the and Hunt 1983; Mock 1984; Evans and McMahon 1987; size dierences between siblings are large, the oldest Drummond et al. 1986; Drummond and GarcõÂ a chick may quickly intimidate its sibling by a low number Chavelas 1989), but not in others (Mock 1985 and Mock of aggressive interactions (Edwards and Collopy 1983), et al. 1987 in herons; R.E. Simmons unpublished data thus explaining the relatively low frequency of ®ghting for Wahlberg's eagle Aquila walbergi). My results sug- observed in asynchronous nests (Mock and Ploger 1987; gest that hatching asynchrony eectively facilitates the Forbes 1991a). However, when this size dierence is too early death of last-hatched chicks, and that the brood high, the small chick may suer serious injuries, may be reduction process is regulated by the size dierence be- rejected from the nest, or crushed by its much larger tween chicks and by food availability (Bortolotti 1986a, sibling. This may explain the high cainism rate in b). However, large hatching asynchronies may also in- asynchronous nests (see also Werschkul 1979; Haydock duce deaths unrelated to food abundance. and Ligon 1986; Mock and Ploger 1987; Amundsen and Synchronous hatching may also increase parental Stokland 1988). The large size disparities between early- eort in some species, because parents must provide hatched chicks and third-hatched chicks in three-chick more food for the same number of chicks due to in- broods would also explain why the wounding rate in creased energy expenses induced by enhanced sibling third chicks was similar to that of ®rst/second chicks, rivalry (Mock and Ploger 1987; Wiebe and Bortolotti although sibling aggression involving third-hatched 1994; Osorno and Drummond 1995). In black kites, the chicks was rarely observed (a lower frequency of ag- degree of hatching asynchrony did not aect average gression would result in a similar wounding rate when daily biomass found in the nests, suggesting that in this size disparities are large). species, synchronous hatching did not impose a cost on parents in the form of increased foraging eort. Optimal asynchrony, from the parental point of view, Sibling aggression and food availability would be intermediate between the maximal and mini- mal possible hatching asynchronies, the pattern indeed Mean prey biomass was higher in three- than in two- observed in control nests (Table 1). In species with fac- chick broods, probably re¯ecting the higher food de- ultative siblicide, this could be a compromise between mand of larger broods, a possible adjustment of parental high hatching asynchrony, promoting over-large size eort to current brood size (Forbes 1993; RodrõÂ guez- dierences leading to high nestling mortality, and low GironeÂ s 1996), and/or the better quality of pairs raising asynchrony increasing sibling aggression and delaying larger broods (VinÄ uela 1991, unpublished data). Mean the appearance of size hierarchies (Mock and Ploger prey biomass was higher in nests that did not lose any 1987; Osorno and Drummond 1995). However, other chick from starvation/siblicide, an expected result given factors could also contribute to shaping optimal hatch- that feeding rates are the main factor regulating pro- ing asynchrony (VinÄ uela, unpublished data). ductivity in raptors (Newton 1979), and birds in general (O'Connor 1984). The relationship between aggressive behaviour and food availability was less clear. A signi- Parental behaviour and parent-ospring con¯ict ®cant negative correlation was found between early aggressiveness (chicks younger than 10 days) and prey Female black kites were observed apparently trying to biomass. However, the ratio of wounds on the chicks reduce sibling aggression during feeding bouts. This was negatively correlated with prey biomass only when kind of behaviour has been reported, to my knowledge, considering the nests with mortality. This may be be- only for the Antarctic skua (Catharacta maccormicki, cause food was not a limiting factor in nests without Young 1963; Spellerberg 1971), and the bald eagle mortality. In fact, in some successful nests, large (Haliaetus leucocephalus, Gerrard and Bortolotti 1988), amounts of surplus food not consumed by the chicks although O'Connor (1978) suggested the possible exis- were found. This could be typical in a species whose tence of similar mechanisms in three other species (Grus feeding ecology is based on sporadic overabundant re- canadensis, Sula dactylatra and Sula leucogaster). Fur- sources (in my study area, the spring breeding peaks of thermore, preferential feeding of last-hatched chicks was abundance of young rabbits or waterfowl, dying/dead also observed. In facultatively siblicidal species, the oc- 42 currence of siblicide may depend basically on the hunger 1983; Braun and Hunt 1983; Ferguson and Sealy 1983; condition of the largest chick/s, the adults leaving it to Horsfall 1984; Stamps et al. 1985; Gottlander 1987), as their older chick to ``take the decision'' depending on its well as cases of parents actively promoting the death of own physical condition (which could be a good indicator last-hatched chicks by an uneven distribution of food of food availability), since they do not interfere in the (Drummond et al. 1986; Drummond and GarcõÂ a ®ghts and do not preferentially feed any chick (review in Chavelas 1989) or by infanticide (Newton 1978; Urrutia O'Connor 1978; see also Drummond et al. 1986; and Drummond 1990). The available information is still Drummond and GarcõÂ a Chavelas 1989; Forbes 1993; too scarce to correlate the appearance of these con- Anderson and Ricklefs 1995). However, in a highly trasting behaviours with other ecological features of the opportunistic predator, exploiting especially brief situa- species (Drummond and GarcõÂ a Chavelas 1989; Forbes tions of resource overabundance, the hunger of the large 1993; Nilsson 1995), but it is suggestive that two of the chick may not be a good indicator of the ability to rear few bird species that show parental behaviours con- more or fewer chicks, because periods of food abun- ducted to reduce sibling aggression are opportunist dance and scarcity alternate during the nestling period predators/carrion eaters. (see Mock et al. 1987). Under these circumstances, the optimal strategy for the parents would be to prolong as long as possible the life of all the chicks, in the expec- Quality of senior chicks tation of possible food overabundance in the future (Temme and Charnov 1987; Bryant and Tatner 1990). Cainistic chicks had similar size and condition to senior This would explain the appearance of behaviours aimed chicks in multiple broods without mortality. Senior at distributing the available food between all the chicks chicks in multiple broods were in better condition that (even only 24±48 h before the death of the smallest single chicks surviving from multiple broods, and senior chick), as well as the reduced growth rate or ®nal size of chicks in broods without mortality were larger and in surviving chicks in broods in which the last-hatched better condition at ¯edging than senior chicks in broods chick died, noted especially in good years (see also He- where a chick starved. This result supports the basic idea bert and Barclay 1986). The high resistance to food from which Simmons' hypothesis was born: by killing its deprivation could be part of this strategy to protract the sibling early in the nestling period, a senior chicks avoids life of the chicks (VinÄ uela and Ferrer 1997), as could be a risk of reaching ¯edging in poor condition. the intermediate degree of hatching asynchrony, since The condition of senior ¯edglings was aected by an age at death was older in control than in experimental interaction between year and mortality. In a year with nests. high mortality by starvation and bad breeding condi- This strategy of resource distribution during times of tions due to unfavourable weather and low availability scarcity could induce the appearance of a parent-o- of diseased rabbits (1988; see Fig. 4 and VinÄ uela and spring con¯ict over brood reduction (O'Connor 1978; Veiga 1992), senior chicks in nests where a chick starved Forbes 1993; Nilsson 1995): the optimal strategy for attained a similar condition as those in nests without every chick would be to optimise its own survival and mortality. In contrast, 1987 was a good year for breed- growth, not to share resources with its smaller siblings at ing during the whole nesting season, and 1989 was in- the expense of its own growth. This would be especially termediate, with good conditions early in the season, but true in species with highly variable provisioning rates poorer conditions later (this explaining the smaller size (Forbes 1991b, 1993; Forbes and Ydenberg 1992; Rod- and poorer condition of senior chicks in 1989; VinÄ uela rõÂ guez-GironeÂ s 1996). Under such circumstances, theo- and Veiga 1992). This result suggests that two mecha- retical models predict the appearance of an ``anticipated nisms to regulate productivity are simultaneously acting response'', and the chicks would be aggressive even in this species, brood reduction and variation in growth when food is not a limiting factor (Stinson 1979; Mock rate or ®nal size. When conditions are especially poor, and Parker 1986; Mock 1987; Mock et al. 1987; Forbes early brood reduction may allow parents to raise high- 1991b; Forbes and Ydenberg 1992), explaining the oc- quality senior chicks (1988). When conditions are better, currence of cainism. Also, in these cases of parent-o- brood reduction would be delayed, as the parents try to spring con¯ict, the appearance of parental ``stratagems'' keep alive all the chicks by distributing resources, but at aimed at attaining the parental objectives are expected: the cost of reduced growth rate or ®nal size (1987 and in this context, for example, the preferential feeding of 1989). Rearing a higher number of chicks may have small chicks. The main remaining question in this kind negative consequences on chick growth (e.g. Anderson of situation, not answered here, would be how the par- 1990a), especially for later-hatched, but also for domi- ents estimate the physical condition of every chick in the nant chicks (Moreno et al. 1998). The strategy to pro- brood, or how and when they ``decide'' to let the small long the life of all chicks, as well as a lower feeding rate chick die. in some broods (Table 5), would explain the large dif- Preferential feeding of smallest chicks has been de- ference in size and condition between senior chicks in scribed for other groups of birds (Bengtsson and RydeÂ n broods with or without mortality during good years. 43

Test of Simmons' hypothesis mons (1991), there may be a continuum from raptor species where siblicide is mainly related to food-regu- Simmons (1988) predicted that cainism should be fre- lated brood reduction and parent-ospring con¯ict quent in saturated populations of facultatively siblicidal (facultatively siblicidal such as black kites), to species species. However, subadult territory occupancy would where siblicide may be more related to the high-quality indicate population instability, and cainism should occur chick demands proposed by Simmons. less frequently. Population instability could explain the low frequency of cainism during 1988, but the black kite Acknowledgements I greatly thank all the people who helped me population in 1989 can be considered saturated, because during ®eld work, especially Javier LoÂ pez Redondo for his observations from the blinds. JoseÂ Pablo Veiga provided helpful criti- it reached one of the highest densities known for the cisms and suggestions during ®eld work and on previous drafts of species, and no additional population growth was de- the manuscript. This is a contribution to the Research Project tected in subsequent years. However, the lowest fre- PB87-0405 of the DireccioÂ n General de InvestigacioÂ n CientõÂ ®ca y quency of cainism was found in that year. I do not have TeÂ cnica. During this work I was supported by a predoctoral fellowship from P.F.P.I., Ministerio de EducacioÂ n y Ciencia. During any clear explanation for the higher frequency of cain- the ®nal analyses and writing, support was provided by a Fulbright ism in 1987, but I have not considered in this work one Postdoctoral Fellowship at Yale University and by National Sci- of the main factors that may facilitate the occurrence of ence Foundation grant no. IBN-9407349 to S.R. Beissinger. cainism, namely the frequency with which the female is Comments by T. Amundsen, J.M. Aparicio, S.R. Beissinger, C.C. absent from the nest (Newton 1977, 1979; Anderson St. Clair, L.S. Forbes, J. Moreno, two anonymous referees and, especially, R.E. Simmons improved previous versions of the 1990a). Perhaps during 1987, some factor, such as scarce manuscript. I declare that all the manipulations included in this food during the early nestling period or increased dis- paper were done with the necessary permissions and comply with turbance near the nests, induced longer or more frequent the Spanish laws on scienti®c research and nature conservation. absences of the female, facilitating higher levels of sibling aggression. Simmons also predicted that under conditions of References population instability, cainism should be more frequent in smaller broods. The opposite was found in the black Amundsen T, Slagsvold T (1991) Hatching asynchrony: facilitating kite. The higher frequency of cainism in three-chick adaptive or maladaptive brood reduction? 20th Int Ornithol broods may be explained simply by the higher hatching Congr, pp 1707±1719 asynchrony of those clutches, because cainism was also Amundsen T, Slagsvold T (1996) Lack's brood reduction hypoth- more frequently observed in experimentally asynchro- esis and avian hatching asynchrony: what's next? Oikos 76:613± 620 nised broods. Amundsen T, Slagsvold T (1998) Hatching asynchrony in great tits: Simmons (1988) also proposed that under strong a bet-hedging strategy? Ecology 79:295±304 population pressure, the traits favouring the occurrence Amundsen T, Stokland JN (1988) Adaptive signi®cance of asyn- of cainism should be enhanced. However, I did not ®nd chronous hatching in the shag: a test of the brood reduction larger intraclutch egg size variation, longer hatching hypothesis. J Anim Ecol 57:329±344 Anderson DJ (1989) The role of hatching asynchrony in siblicidal asynchronies, or longer laying intervals when the pop- brood reduction of two booby species. Behav Ecol Sociobiol ulation of black kites approached saturation. Although I 25:363±368 did not systematically record the frequency of aggressive Anderson DJ (1990a) Evolution of obligate siblicide in boobies. 2. interactions between neighbouring pairs, these clearly Food limitation and parent-ospring con¯ict. Evolution 44:2069±2082 increased from 1987 to 1989. This could explain the re- Anderson DJ (1990b) Evolution of obligate siblicide in boobies. 1. duction in clutch size from 1987 to 1989. But, since A test of the insurance-egg hypothesis. Am Nat 135:334±350 cainism was not higher in smaller clutches, this cannot Anderson DJ (1995) The role of parents in siblicidal brood re- be considered as evidence supporting Simmons' hy- duction of two booby species. Auk 112:860±869 Anderson DJ, Ricklefs RE (1995) Evidence of kin-selected toler- pothesis. ance by nestlings in a siblicidal bird. Behav Ecol Sociobiol The results obtained in this population of black kites 37:163±168 do not completely invalidate Simmons' hypothesis, be- Bengtsson H, Ryden O (1983) Parental feeding rate in relation to cause the black kite may not be an adequate species to begging behaviour in asynchronously hatched broods of the test it. Black kites are semi-colonial raptors, rarely great tit Parus major. Behav Ecol Sociobiol 12:243±251 Bortolotti G (1986a) Evolution of growth rates in eagles: sibling maintain feeding territories (but see VinÄ uela et al. 1994), competition versus energy considerations. Ecology 67:182±194 and may reach some of the highest nesting densities Bortolotti G (1986b) In¯uence of sibling competition on nestling known for raptors. Simmons presented his hypothesis sex ratios of sexually dimorphic birds. Am Nat 127:495±507 speci®cally to explain cainism in strongly territorial Braun BM, Hunt GL (1983) Brood reduction in black-legged kit- tiwakes. Auk 100:469±476 raptors, such as eagles, and he has shown recently in- Bryant DM, Tatner P (1990) Hatching asynchrony, sibling com- teresting evidence in the Wahlberg's eagle supporting his petition and siblicide in nestling birds: studies of swiftlets and ideas (Simmons 1993, 1997). However, my work shows bee-eaters. Anim Behav 39:657±671 that cainism may appear, at least at a low frequency, in a Cramp S (ed) (1980) The birds of the western Palearctic, vol I. Oxford University Press, Oxford context dierent to that outlined by Simmons' hypoth- Delannoy CA, Cruz A (1988) Breeding biology of the Puerto-rican esis that, consequently, is not a universal explanation for sharp-shinned hawk (Accipiter striatus venator). Auk 105:649± the phenomenon. Following Newton (1977) and Sim- 662 44

Delibes M, GarcõÂ a L (1984) HaÂ bitos alimenticios del Milano Real Mock DW (1984) Infanticide, siblicide and avian nesting en DonÄ ana durante el periodo de crõÂ a. Ardeola 31:115±121 mortality. In: Hausfaster G, Hrdy SB (eds) Infanticide: com- Drummond H (1987) A review of parent-ospring con¯ict and parative and evolutionary perspectives. Aldine, New York, pp brood reduction in Pelecaniformes. Col Waterbirds 10:1±15 3±30 Drummond H, Garcia Chavelas C (1989) Food shortage in¯uences Mock DW (1985) Siblicidal brood reduction: the prey-size hy- sibling aggression in the blue-footed booby. Anim Behav pothesis. Am Nat 125:327±343 37:806±819 Mock DW (1987) Siblicide, parent-ospring con¯ict, and unequal Drummond H, GonzaÂ lez E, Osorno JL (1986) Parent-ospring parental investment by egret and herons. Behav Ecol Sociobiol cooperation in the blue-footed booby (Sula nebouxii): social 20:247±256 roles in infanticidal brood reduction. 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