Ó Springer-Verlag 1999
Behav Ecol Sociobiol (1999) 45: 33±45
ORIGINAL ARTICLE
Javier VinÄuela
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 could act to reduce sibling rivalry or promote the death of last-hatched chicks. The pattern of hatching asynchrony was experimentally altered in the black kite Milvus migrans. Hatching asynchrony in control broods was intermediate between those of experimentally synchronised and asynchronised broods. Sibling aggression and wounds on the chicks were more commonly observed early in the nestling period and in synchronous nests. Serious injuries were observed on last-hatched chicks in asynchronous nests, as were observations of intimidated or crushed chicks. Sibling aggression was related to food abundance, but some chicks died at an early age in nests with abundant food (cainism). Cainism was more commonly found in asynchronous nests. For species with facultative siblicide, moderate hatching asynchrony could be a compromise between reducing sibling rivalry and avoiding large size dierences between sibs that would result in cainism. Female black kites preferentially fed the smallest chicks and exhibited behaviours to reduce sibling aggression, contrary to observations in other siblicidal species. In a highly opportunistic forager such as the black kite, a strategy may exist to protract the life of all the chicks in the brood, waiting for unpredictable situations of food overabundance. This would induce the appearance of a parentospring con¯ict over brood reduction, re¯ected in the existence of a possible anticipated response by some of the chicks (cainism) and in the appearance of special behaviours by the parents to selectively feed smaller chicks or reduce sibling aggression. In this facultatively siblicidal species, cainism does not seem to be the ®nal stage of an evolutionary trend favouring the raising of
J. VinÄuela (&) Departamento de Ecologõ a Evolutiva Museo Nacional de Ciencias Naturales, (C.S.I.C.) Jose Gutierrez Abascal 2, E-28006 Madrid, Spain e-mail:
[email protected], Tel.: +34-1-4111328, Fax: +34-1-564078
high-quality chicks, but a manifestation of a parentospring con¯ict over brood size. Key words Hatching asynchrony á Sibling aggression á Nestling mortality á Parent-ospring con¯ict á Milvus migrans
Introduction Sibling aggression and hatching asynchrony are common in raptors (Newton 1979), and may promote siblicide (Simmons 1988). Hatching asynchrony could reduce sibling aggression between size-matched chicks (Hahn 1981), allowing the establishment of a size hierarchy with a minimum of aggressive interactions. Alternatively, it could promote the death of last-hatched chicks by establishing large size dierences between siblings, since in obligately siblicidal species (those in which >90% of last-hatched chicks die; Simmons 1988), hatching asynchrony is higher than in facultative species (those in which siblicide occurs in 95% of days) from the start (mid-March) to the end (end of July) of the breeding seasons of 1987, 1988 and 1989. Nests were visited daily during laying and eggs were marked with felt pens. Laying was considered to be ®nished when the third egg was found or if 4 days elapsed since the previous one was found. After laying, nests were not visited again until 28±30 days after the date of laying of the ®rst egg. Nests were visited daily during hatching, and the chicks individually marked under the wing with felt pens. Brood size at hatching varied between one and three chicks. Nests in which only one chick hatched have not been considered, unless otherwise indicated in the text.
35 Hatching asynchrony 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 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 held until 3 days after the second egg was laid, when they were returned to the nest. Third-laid eggs were marked when found, but not removed. Experimental clutches were alternatively assigned to one of two treatments: (1) asynchronous clutches had eggs maintained during the removal period in incubators at 37±38 °C, with water containers below the eggs (Campbell and Flood 1977; Burnham 1978, 1983), and (2) synchronous clutches were not incubated, but maintained at ambient temperature during the removal period. Eggs in both treatments were turned 180° twice daily. Hereafter, experimental nests are named asynchronous and synchronous, while nests with unaltered hatching asynchrony are named controls. Hatching asynchrony was de®ned as the time elapsed in hours between hatching of ®rst and last eggs in the clutch, and was estimated following a variation of the method of Stokland and Amundsen (1988) (VinÄuela 1996). For the analyses of variation in hatching asynchrony in control nests among years, only the cases in which the ®rst- and last-laid eggs in a clutch hatched have been included. For all analyses, hatching order has been considered instead of laying order (in most of the synchronous nests hatching order was opposite to laying order; VinÄuela 1997a). Hatching asynchrony of control nests was intermediate between those of experimental synchronous and asynchronous nests (Table 1; VinÄuela 1996). Nestling mortality All nests were visited 2±3 days after hatching of last chicks, and every 4±7 days (mostly every 5 days) thereafter until the end of the nestling period. On each nest check after hatching, I renewed the marks on the chicks and recorded cases of mortality. In some cases of predation, clues from the predator were found (mainly tawny owls Strix aluco), and in all of them the complete brood was depredated. Total brood losses in raptors are usually related to predation (Newton 1979). All nests in which there was nestling mortality due to other causes (predation, abandonment and nest collapse) have been excluded from the analyses of nestling mortality by starvation or siblicide. However, three cases in which the broods were depredated near the end of the nestling period, well beyond the maximum age of death by starvation or siblicide recorded during the 3 study years, have been considered as nests without starvation or siblicide mortality. Black kite chicks have a high resistance to food deprivation, often suering important growth delays due to protracted periods of food scarcity (Hiraldo et al. 1990; Veiga and Hiraldo 1990). This facilitated the detection of this kind of mortality, as the chicks suered evident retarded growth and were extremely emaciated before death. Age of death for every chick was estimated assuming that death occurred half way between the day on which the death was detected and the previous visit. For the three broods with three chicks where Table 1 Hatching asynchrony (h) in black kite broods of two and three chicks. Variation between control nests (natural hatching patterns) and experimental nests (hatching synchronised or asynchronised by altering incubation pattern during the laying period). Sample sizes in parentheses Clutch size Treatment Asynchronous
Control
Synchronous
Two eggs 82.4 33.1 (11) 53.9 23.8 (35) 19.8 14.9 (9) Three eggs 108.7 13.7 (4) 89.7 20.9 (23) 34.5 21.4 (4)
two chicks died, the average of ages of death for each sibling was considered. Sibling aggression During 1988 and 1989, aggressive behaviour between siblings just after arriving at the nests was recorded. These attacks were pecks given mostly on the head, especially around the beak and eyes, and on the nape. During these ®ghts, the chicks also apparently tried to twist the neck of their opponent by grasping its head or neck and shaking it strongly from side to side. When aggression was observed, the number of pecks given by the chicks during the ®rst minute after the start of the ®ght was recorded. The number of pecks given by all chicks in a brood during each visit have been pooled. Young chicks (0±10 days old) have no well-developed recognition abilities, and they often begged the observer for food (see Delannoy and Cruz 1988 and Gargett 1990 for similar observations in other raptors). Sibling aggression in raptors occurs especially when the female is absent from the nest (Newton 1979). These absences must be rare during the early nestling period, since brooding in black kites is almost continuous during the ®rst 2 weeks after hatching (Cramp 1980; Koga and Shiraishi 1987; personal observation). Thus, nestling behaviour during early nest checks, just after the female was ¯ushed from the nests, may be a good estimate of the level of aggression. Between 10±20 days of age, the chicks changed their behaviour, remaining crouched down, adopting defensive attitudes, or even attacking the intruder, but rarely fought each other (see below). Those cases in which the older sib in a brood was lying on a smaller sibling, or the smallest chick was clearly intimidated on the nest rim (head lowered and body tightly crouched down, as observed in the ``loser'' chicks after a ®ght) were also recorded. The occurrence of wounds on the chicks was also noted on every nest check. Only recent wounds and those partially scarred, but not recorded during the previous visit, were considered. I counted the total number of wounds found on all the chicks in a brood and at every nest check. In the most extreme cases, the back of the injured chick was plucked and bloody (see Meyburg 1974), or the eyes were so seriously wounded, the chick could no longer open them. A score of 12 wounds was assigned to these large injuries (one more that the maximum number of discrete wounds found per chick during the whole study). The nestling period was divided into nine periods (Fig. 1), depending on the age of the older chick in the brood. When more than one visit was made in one of these age periods, averages for all the visits within each time period were calculated. To analyse the eect of brood size on sibling aggression, the averages of attacks/ wounds for ®rst- and second-hatched chicks and attacks/wounds for third-hatched chicks were calculated (Table 2). To avoid pseudoreplication, averages of each variable for each nest were used in all the analyses, except those relating behaviour and age of the chicks. For the analyses involving the variables ``mean number of attacks'' and ``mean number of wounds'', nonparametric statistics were used, because inspection of plots and preliminary analyses on transformed and untransformed variables did not provide evidence of normality. During every nest check, prey remains at the nest were recorded (see VinÄuela and Veiga 1992 for details). Black kites have very poorly developed nest-cleaning habits, and most prey remains are not removed from the nests, so they may provide a reasonable estimate of food provisioning for comparative purposes (VinÄuela 1991). On every nest check, prey remains without meat were removed, and those that could still be eaten marked, to avoid repeating records in subsequent visits. Biomass of prey was estimated from values reported in the bibliography and from my own ®eld measurements of fresh and entire prey (VinÄuela 1991). To estimate biomass of rabbits, the main prey in this area, tarsus of rabbit remains were measured, and biomass estimated following Delibes and GarcõÂ a (1984). Total estimated biomass recorded at every nest 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
Fig. 1 Variation during the nestling period of mean number of wounds found on the chicks (a) and mean number of attacks observed during nest checks (b). Values are means S.E. for every age period (referred to the age of the older chick in the brood). Number of nest visits above bars
Table 2 Attacks and wounds observed in broods of two chicks, 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 10 days (Attacks). Number of broods and means SD for each category. Averages with dierent superscripts are signi®cantly different (Mann-Whitney U-tests, P < 0.05) Two chicks
Three chicks 1st±2nd
All nests Attacks Wounds Control nests Attacks Wounds
44 1.1 1.3 26 0.2 1.2
2.8ab 1.7 0.5ab 1.7
18 1.5 1.2 12 0.6 0.7
3rd
2.9a 1.5
0.2 0.5b 1.1 1.6
1.5a 0.6
0b 0.7 1.2
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 (VinÄuela 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 VinÄuela 1993, 1997b). In the last study year, one of the highest population densities recorded for this species was reached (VinÄuela 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 VinÄuela 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 proposed by Slagsvold et al. (1984), but I considered the relative size of last-laid eggs with respect to the largest egg in the clutch, instead of the average mass of the clutch (see VinÄuela 1997b). This index was mass of last-laid egg ´ 100/mass of largest egg (the ®rst in most two-egg clutches and the second in most three-egg clutches; VinÄuela 1997b).
Results Chick mortality by starvation and siblicide The productivity of two- and three-egg clutches, depending on the treatment, is shown in Table 3. Five chicks were found dead in the nest with wounds in the head or the back, of which three also had their neck apparently twisted. In two asynchronous nests, last-hatched chicks with a full crop were found dead below their much larger siblings. In these cases, the small chick was probably crushed or asphyxiated, another kind of siblicide, as previously suggested for other species of raptors (Wendland 1958 in Meyburg 1974). In eight broods, the smallest chick was observed intimidated on the nest rim. Four of
37 Table 3 Mean SD number of chicks ¯edged in broods of the black kite during 1988 and 1989 (sample size in parentheses) with variation in original clutch sizes (one-egg clutches excluded) and treatment. Only broods where more than one chick hatched are shown. Broods where chicks were lost due to causes other than brood reduction (predation, abandonment or nest collapse) were excluded
1989, cainism occurred more frequently in asynchronous (4 cases in 14 nests) than in control nests (2 cases in 34 nests) (Fisher exact test, P 0.04), but there was no dierence between control and synchronous nests (no cases in 11 nests).
Clutch size
Treatment
Number of ¯edglings
Age at death
Two eggs
Asynchronous Control Synchronous Asynchronous Control Synchronous
1.5 1.5 1.7 1.6 2.1 2.2
Three eggs
0.5 0.5 0.5 0.5 0.6 0.7
(4) (19) (6) (8) (17) (6)
these chicks were found dead or dying on the ground below the nests 24±72 h later. Similar cases have been described for other raptor species and are considered another form of siblicide (Meyburg 1974). The existence of siblicide was also con®rmed by direct observations. I witnessed the older chick of a two-chick brood pecking its sibling for 4 h in the evening, after 12 h without food. The next morning the smaller chick appeared partially eaten in the nest. Five chicks younger than 5 days disappeared from nests, and have also been considered as cases of siblicide, because they were partial losses unrelated to abandonment or nest collapse, and predation caused complete loss of the brood, as observed in other raptors (Newton 1979). 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 cases assigned to siblicide, the dead chicks had starvation symptoms. Thus, both kinds of mortality were clearly associated, as observed in other raptor species (Newton 1979). However, in the remaining 11 cases of siblicide, the chicks died without having showed signs of starvation or retarded growth, at an early age (Fig. 2), and in nests where food was plentiful (estimated daily biomass in the nests from hatching of the ®rst chick to the day on which the death was discovered: 223 183 g, range: 50±673). These cases are considered cainism, following Simmons (1988). During 1988 and
Fig. 2 Frequency distribution of the age at death by starvation (hatched bars) or siblicide (white bars)
Most of the chicks died from starvation or siblicide at a young age (27% of deaths aected chicks younger than 5 days; Fig. 2). A multifactorial ANOVA revealed signi®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 1987 (6.1 11 days, n 7) than in 1988 (12.2 8.2 days, n 16) or 1989 (14.1 9 days, n 15) (partial F2,32 7.2, P 0.003), because cainism was more frequently observed during 1987 (see below), and chicks lost due to cainism died at a younger age than chicks lost to starvation (F1,36 23.4, P < 0.001; Fig. 2). Chicks in control broods tended to die at an older age (13.4 10.1 days, n 18) than chicks in asynchronous (8.9 6.5 days, n 10) or synchronous broods (8.6 8.6 days, n 3) (partial F2,32 3.2, P 0.055). Age at death was lower in three-chick (8.2 7.8 days, n 18) than in two-chick broods (15.1 9.5 days) (partial F1,32 5.2, P 0.03). Sibling aggression and hatching asynchrony The variables used to estimate the levels of sibling aggression did not signi®cantly vary from 1988 to 1989 (Mann-Whitney U-tests of averages for each brood; sibling aggression: Z 0.97, P 0.33; wounds: Z 0.8, P 0.42; `crushing': Z 1.33, P 0.18; `nest rim': Z 1.2, P 0.14), so data from both years have been pooled for subsequent analyses. The chicks exhibited aggressive behaviour towards their siblings as early as the day of hatching. Sibling 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 between two- and three-chick broods, even when considering 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
Fig. 3 Mean + SE number of attacks (white bars) and wounds (hatched bars) observed during nest checks in control (n 38), experimentally synchronised (n 12) and synchronised (n 12) broods. Averages for every brood during the nestling period
The mean number of observations of last-hatched chicks below their larger siblings was higher in asynchronous broods, although signi®cant dierences were found only when comparing asynchronous and synchronous broods (Z 2.09, P 0.037, Table 4). The mean number of observations of chicks intimidated on the nest rim tended to be higher in asynchronous than in control (Z 1.9, P 0.055) or synchronous broods (Z 2.13, P 0.033) (Table 4). Brood size did not signi®cantly aect either of these two variables (crushing: Z 0.04, P 0.96; nest rim: Z 1.3, P 0.19). The mean number of wounds per visit increased to a maximum when the older chick was 15±19 days old and declined thereafter (Kruskal-Wallis, H 39.4, P < 0.001, Fig. 1). The average number of wounds was higher in synchronous than in control nests (Z 2.13, P 0.03), but not higher than in asynchronous nests (Z 1.1, P 0.27) (Fig. 3). Asynchronous nests also had a relatively high mean number of wounds, but the dierence with control nests was not signi®cant (Z 0.17, P 0.86). This probably re¯ects a high variance in the mean number of wounds found in 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 nest rim with a dislocated leg, and three chicks with large plucked and blooded areas on the back and head). However, wounds were rarely seen in other asynchronous nests, probably due to early intimidation of lasthatched siblings in nests where food was abundant and, consequently, chick aggressiveness was low. The mean Table 4 Mean (SD) number of observations of oldest chicks lying down on their smaller sibling (Crushing), and smallest chicks intimidated on the nest rim (Nest rim) in control and experimentally synchronised or asynchronised broods. Averages for each brood during the nestling period
Asynchronous (n 12) Control (n 38) Synchronous (n 12)
Crushing
Nest rim
0.11 0.21 0.04 0.08 0
0.10 0.17 0.02 0.07 0
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 true when considering only the ®rst 10 days of the nestling period (203 131 g/day; range: 7±633). The average 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 no-mortality and cainistic nests (Table 5). Biomass was higher in three-chick (250 125 g/day) than in twochick (191 111 g/day) broods (two-way ANOVA, mortality: F2,56 5.9, P 0.005; brood size: F1,56 6.8, P 0.011). Average daily biomass was not significantly aected by the year (1988: 186.5 110 g/day; 1989: 223 121 g/day; F1,60 1,4, P 0.23) or treatment (asynchronous broods: 194.5 108 g/day; control broods: 215 115 g/day; synchronous broods: 200 139 g/day; F2,59 0.17, P 0.84). Mean prey biomass was negatively correlated with average number of attacks on chicks younger than 10 days (rs )0.25, P 0.051, n 62). No correlation was found between prey biomass and mean number of wounds (rs )0.15, P 0.23, n 62) for all nests pooled, but when considering only the nests with mortality from starvation, this correlation was signi®cant (rs )0.43, P 0.027, n 26). Broods that lost some chicks by cainism or starvation had higher rates of wounding than broods without mortality (Table 5) but, although the nests with cainism showed high rates of aggression (Table 5), no signi®cant dierences were found for this variable. Quality of senior chicks Final size and condition of senior chicks were highly variable, as might be expected in a species with a highly Table 5 Mean daily biomass, estimated from prey remains found 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. Averages for each brood type during the nestling period. Data pooled for 1988 and 1989. Means with dierent superscripts are signi®cantly dierent (ANOVA and post-hoc Tukey HSD test for biomass, and Mann-Whitney U-tests for attacks and wounds)
Biomass (g) Attacks Wounds
No mortality (n 29)
Starvation (n 26)
Cainism (n 5)
246 117a 1.4 3.2 1 1.2a
165 98b 0.9 2.5 1.9 2.1b
246 152a 3.1 4.5 2.5 1.8b
39
¯exible growth (Hiraldo et al. 1990; VinÄuela and Veiga 1992; Table 6). Tarsus length was not signi®cantly affected 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 (VinÄuela 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 found signi®cant eects of year (F2,70 5.5, P 0.006) and brood size (F2,70 14.4, P < 0.001) on ¯edging mass, but not of mortality or treatment. The same analysis with ¯edgling condition as dependent 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 similar condition in broods with or without mortality. In contrast, senior chicks in broods where a chick had starved were in poorer condition than those in broods without mortality during 1987 and 1989 (Fig. 4).
Table 6 Fledging mass, tarsus length and ¯edgling condition [residuals of the regression of Fledging weight on (tarsus length)3] of senior chicks of black kites in broods where more than one egg hatched. Variation among years, mortality [0 broods without mortality, 1 broods where a chick was lost due to starvation, 2 broods where cainism (death of young chicks not associated with food scarcity) occurred], ®nal brood size, and treatment (A experimental asynchronous nests, C control nests, S experimental synchronous nests). Means SD. Means with dierent superscripts are signi®cantly dierent (ANOVAs and Tukey HSD posthoc test, P < 0.05). Sample sizes are given in parentheses Variable
Mass
Tarsus
Year
736 77a 737 62a 694 85b 747 64a 670 89b 725 44ab 661 87a 739 63b 755 46b 713 107 709 75 759 53 717 79 415±888
57.2 56.9 57.1 57.3 56.7 57.0 56.9 57.1 57.3 57.6 56.9 57 57.1 52±62
1987 (17) 1988 (24) 1989 (35) Mortality 0 (39) 1 (26) 2(10) Brood size 1 (24) 2 (40) 3 (12) Treatment A (12) C (53) S (11) Total (76) Mean Range
Condition 1.6 1.9 1.7 1.9 1.8 1.0 1.3 2 1.6 1.3 1.9 1.5 1.7
11.7 18 )28.5 20.8 )44.8 3.9 )56.7 16.3 28.8 )18 )10.6 37.8 )4.8 )312±128
66.3ab 54.1a 83.1b 55.3a 88.7b 54.2ab 88a 53.9b 44.5b 108.4 68.2 38.1 73.4
Fig. 4 Condition at ¯edging (mass/tarsus length3) of senior chicks of black kites related to the study year and occurrence of nestling mortality (white bars no mortality, hatched bars starvation mortality, black bars cainism). Groups with dierent letters above bars are signi®cantly dierent (ANOVA and Tukey HSD post-hoc test). Sample sizes are also given above bars
Test of Simmons' hypothesis Cainism occurred more frequently in three-chick (23% of 31 nests) than in two-chick broods (7% of 56 nests) (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. The laying interval between second and third eggs varied between 2 and 4 days, and in most cases was 3 days (71%) (mean SD 3.1 0.5, n 46). The laying interval did not show any signi®cant variation among years (F2,45 0.9, P 0.4), and the relative size of last laid eggs did not vary signi®cantly among years (F2,124 0.06, P 0.94). Clutch size decreased from 1987 (2.8 0.4, n 21) to 1988 (2.4 0.6, n 50) and 1989 (2.2 0.5, n 67) (F2,135 9.4, P < 0.001). This could be due to the increase in inexperienced birds among breeders from 1987 to 1989 (VinÄuela 1993), since inexperienced black kite pairs had smaller clutches (experienced: 2.6 0.5, n 69; inexperienced: 2.2 0.5, n 69; F 22.7, P < 0.001). However, a two-way ANOVA revealed independent effects of breeder experience (F1,132 11.6, P < 0.001) and year (F2,132 10.6, P < 0.001). Hatching asynchrony of control nests decreased from 1987 (85.6 21.2 h, n 13) to 1988 (78.6 29.9 h, n 11) and 1989 (57.2 28.9 h, n 23) (F 5.2, P < 0.01), but this may be a consequence of the interannual variation in clutch size, since hatching asynchrony in this species increases with clutch size (Table 1). A two-
40
way ANOVA of hatching asynchrony on clutch size and year revealed a clear eect of clutch size (F 22.5, P < 0.001), but not of year (F 1.1, P 0.34). Observations of behaviour of parents and chicks Sibling aggression was not recorded in a three-chick brood observed for 26 h when the chicks were 25± 40 days old. In contrast, in the ®ve nests observed when the chicks were 4±10 days old (two two-chick broods and three three-chick broods), ®ghts between siblings were observed frequently, whenever the female was out 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 chicks with the head blooded after the ®ght) were observed between the ®rst and second chick of two threechick broods (estimated hatching asynchronies of 31 and 7 h). In contrast, in a two-chick asynchronous brood (estimated hatching asynchrony 85 h.) the ®ghts were brief, as the largest chick intimidated its sibling after one to three pecks. Aggressive behaviour of chicks during feeding bouts was also remarkably dierent depending on hatching asynchrony and brood size. In three-chick broods (n 3), the two largest chicks (®rst and second hatched) tried to exclude the third-hatched sibling from feeding, as they pecked it on the head whenever it tried to rise, as happened in the two-chick asynchronous brood. In contrast, the ®rst- and second-hatched chicks of three-chick broods usually did not ®ght during feeding bouts, but tried to be the ®rst to get the food morsels from the beak of the female, or they tried to snatch the food from their sibling's beak. However, in almost all the feeding bouts observed (31 out of 39), the female was able to give some food to the smallest chick, even during two feeding bouts 24±48 h before the last-hatched chicks died in two nests. Two behaviours of the females that resulted in the smallest nestling receiving some food were recorded. The female usually entered the nest on the same side (usually the outer side of the crown of the tree), and the chicks tried to stay as near as possible to that side, struggling to get the favoured position (``jockeying'' behaviours, see Bengtsson and RydeÂn 1983 and Gottlander 1987). In three-chick broods, the two largest siblings always monopolised the favourable position, leaving the smallest chick at the back. During three feeding bouts, the female, after giving some food to the largest chicks, took the prey in her beak and walked around the nest rim until near the smallest chick and fed it until the largest chicks again took the ``®rst-line'' position ahead of the small sibling. On four occasions I observed the female exclusively feed the smallest chick of one three-chick brood and the second-hatched chick of the asynchronous two-chick brood. This occurred after feeding bouts during which
the largest chicks ®lled their crop, but the small one obtained little food. After these feeding bouts, the female 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 up, when the female resuming brooding again. The female repeated this behaviour as many as four times after a ``normal'' feeding bout. During a feeding bout in a three-chick brood, when the two ®rst-hatched chicks were ®ghting strongly, the female pecked the head of the second-hatched chick, and placed herself between the two siblings before resuming feeding.
Discussion Sibling aggression, age and hatching asynchrony Sibling aggression and wounds were frequently observed in young chicks, but rarely in old ones. The reduction in the frequency of observations of ®ghts could be due to the change in behaviour of the chicks towards the observer (see Methods). This change in behaviour could also explain why the number of wounds reached a peak later in the nestling period than the number of attacks (Fig. 1). However, the frequency of observation of wounds con®rms a reduction in aggressiveness during the second half of the nestling period. This reduction in aggression as chicks grow older is the rule in birds (Gargett 1970; Meyburg 1974; Mock 1984; Bortolotti 1986a; Drummond and GarcõÂ a Chavelas 1989). Early in the nestling period, the expected bene®ts (in terms of food provisioning) for a siblicidal senior chick are greater than in later stages, so a higher level of aggression would be expected among younger chicks (Forbes and Ydenberg 1992). Sibling aggression was more frequently observed in synchronous nests, as predicted by theory (longer/ stronger ®ghts among size-matched opponents; Maynard Smith and Parker 1976). This result supports the hypothesis that hatching asynchrony may act to reduce sibling rivalry (Hamilton 1964; Hahn 1981), as shown in studies with herons (Fujioka 1985a,b; Mock and Ploger 1987), boobies (Anderson 1989; Osorno and Drummond 1995), ospreys (Forbes 1991a) and American kestrels (Wiebe and Bortolotti 1994). In three-chick broods, sibling aggression between ®rst and second chicks was more frequently observed than aggressions involving third-hatched chicks. Similar arguments may be used in this case, because hatching asynchrony between ®rst and second chicks was smaller that that between second and third chicks, at least in control nests (VinÄuela 1997a, unpublished data). Given that hatching asynchrony did not clearly aect the size or condition of senior chicks (Table 6), it seems that the cost of enhanced sibling rivalry in synchronous nests is mainly re¯ected in the earlier age at death in
41
cases of brood reduction, in a slower growth of chicks in synchronous broods, and in a small size of last-hatched chicks in synchronous nests (VinÄuela 1991, unpublished data). Even in synchronous nests, a size hierarchy could be noted in most cases (VinÄuela 1996), so synchronisation of hatching would simply delay the establishment of the hierarchy at a higher energy cost (slower growth) for the ®nally dominant chick (Osorno and Drummond 1995), or induce earlier mortality/poor growth. Cases of intimidation of the youngest chick and of the large chick lying on its younger sibling were more frequently observed in asynchronous nests. When the size dierences between siblings are large, the oldest chick may quickly intimidate its sibling by a low number of aggressive interactions (Edwards and Collopy 1983), thus explaining the relatively low frequency of ®ghting observed in asynchronous nests (Mock and Ploger 1987; Forbes 1991a). However, when this size dierence is too high, the small chick may suer serious injuries, may be rejected from the nest, or crushed by its much larger sibling. This may explain the high cainism rate in asynchronous nests (see also Werschkul 1979; Haydock and Ligon 1986; Mock and Ploger 1987; Amundsen and Stokland 1988). The large size disparities between earlyhatched chicks and third-hatched chicks in three-chick broods would also explain why the wounding rate in third chicks was similar to that of ®rst/second chicks, although sibling aggression involving third-hatched chicks was rarely observed (a lower frequency of aggression would result in a similar wounding rate when size disparities are large). Sibling aggression and food availability Mean prey biomass was higher in three- than in twochick broods, probably re¯ecting the higher food demand of larger broods, a possible adjustment of parental eort to current brood size (Forbes 1993; RodrõÂ guezGironeÂs 1996), and/or the better quality of pairs raising larger broods (VinÄuela 1991, unpublished data). Mean prey biomass was higher in nests that did not lose any chick from starvation/siblicide, an expected result given that feeding rates are the main factor regulating productivity in raptors (Newton 1979), and birds in general (O'Connor 1984). The relationship between aggressive behaviour and food availability was less clear. A signi®cant negative correlation was found between early aggressiveness (chicks younger than 10 days) and prey biomass. However, the ratio of wounds on the chicks was negatively correlated with prey biomass only when considering the nests with mortality. This may be because food was not a limiting factor in nests without mortality. In fact, in some successful nests, large amounts of surplus food not consumed by the chicks were found. This could be typical in a species whose feeding ecology is based on sporadic overabundant resources (in my study area, the spring breeding peaks of abundance of young rabbits or waterfowl, dying/dead
rabbits in years of high incidence of myxomatosis, dying ®sh or cray®sh when marshes dry out, or sporadic overabundance of rubbish from human activity; VinÄuela 1991; VinÄuela and Veiga 1992). Additionally, the aggressiveness of chicks could be unrelated to food abundance if they exhibit an anticipated response (see below), and in fact, prey biomass at nests with cainism was not dierent from that in nests without mortality. A reinforcement of the aggressiveness of chicks by food scarcity has been reported in several studies (Ingram 1962; Procter 1975; Newton 1977; Poole 1979, 1982; Braun and Hunt 1983; Mock 1984; Evans and McMahon 1987; Drummond et al. 1986; Drummond and GarcõÂ a Chavelas 1989), but not in others (Mock 1985 and Mock et al. 1987 in herons; R.E. Simmons unpublished data for Wahlberg's eagle Aquila walbergi). My results suggest that hatching asynchrony eectively facilitates the early death of last-hatched chicks, and that the brood reduction process is regulated by the size dierence between chicks and by food availability (Bortolotti 1986a, b). However, large hatching asynchronies may also induce deaths unrelated to food abundance. Synchronous hatching may also increase parental eort in some species, because parents must provide more food for the same number of chicks due to increased energy expenses induced by enhanced sibling rivalry (Mock and Ploger 1987; Wiebe and Bortolotti 1994; Osorno and Drummond 1995). In black kites, the degree of hatching asynchrony did not aect average daily biomass found in the nests, suggesting that in this 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, would be intermediate between the maximal and minimal possible hatching asynchronies, the pattern indeed observed in control nests (Table 1). In species with facultative siblicide, this could be a compromise between high hatching asynchrony, promoting over-large size dierences leading to high nestling mortality, and low asynchrony increasing sibling aggression and delaying the appearance of size hierarchies (Mock and Ploger 1987; Osorno and Drummond 1995). However, other factors could also contribute to shaping optimal hatching asynchrony (VinÄuela, unpublished data). Parental behaviour and parent-ospring con¯ict Female black kites were observed apparently trying to reduce sibling aggression during feeding bouts. This kind of behaviour has been reported, to my knowledge, only for the Antarctic skua (Catharacta maccormicki, Young 1963; Spellerberg 1971), and the bald eagle (Haliaetus leucocephalus, Gerrard and Bortolotti 1988), although O'Connor (1978) suggested the possible existence of similar mechanisms in three other species (Grus canadensis, Sula dactylatra and Sula leucogaster). Furthermore, preferential feeding of last-hatched chicks was also observed. In facultatively siblicidal species, the oc-
42
currence of siblicide may depend basically on the hunger condition of the largest chick/s, the adults leaving it to their older chick to ``take the decision'' depending on its own physical condition (which could be a good indicator of food availability), since they do not interfere in the ®ghts and do not preferentially feed any chick (review in O'Connor 1978; see also Drummond et al. 1986; Drummond and GarcõÂ a Chavelas 1989; Forbes 1993; Anderson and Ricklefs 1995). However, in a highly opportunistic predator, exploiting especially brief situations of resource overabundance, the hunger of the large chick may not be a good indicator of the ability to rear more or fewer chicks, because periods of food abundance and scarcity alternate during the nestling period (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 expectation of possible food overabundance in the future (Temme and Charnov 1987; Bryant and Tatner 1990). This would explain the appearance of behaviours aimed at distributing the available food between all the chicks (even only 24±48 h before the death of the smallest chick), as well as the reduced growth rate or ®nal size of surviving chicks in broods in which the last-hatched chick died, noted especially in good years (see also Hebert and Barclay 1986). The high resistance to food deprivation could be part of this strategy to protract the life of the chicks (VinÄuela and Ferrer 1997), as could be the intermediate degree of hatching asynchrony, since age at death was older in control than in experimental nests. This strategy of resource distribution during times of scarcity could induce the appearance of a parent-ospring con¯ict over brood reduction (O'Connor 1978; Forbes 1993; Nilsson 1995): the optimal strategy for every chick would be to optimise its own survival and growth, not to share resources with its smaller siblings at the expense of its own growth. This would be especially true in species with highly variable provisioning rates (Forbes 1991b, 1993; Forbes and Ydenberg 1992; RodrõÂ guez-GironeÂs 1996). Under such circumstances, theoretical models predict the appearance of an ``anticipated response'', and the chicks would be aggressive even when food is not a limiting factor (Stinson 1979; Mock and Parker 1986; Mock 1987; Mock et al. 1987; Forbes 1991b; Forbes and Ydenberg 1992), explaining the occurrence of cainism. Also, in these cases of parent-ospring con¯ict, the appearance of parental ``stratagems'' aimed at attaining the parental objectives are expected: in this context, for example, the preferential feeding of small chicks. The main remaining question in this kind of situation, not answered here, would be how the parents estimate the physical condition of every chick in the brood, or how and when they ``decide'' to let the small chick die. Preferential feeding of smallest chicks has been described for other groups of birds (Bengtsson and RydeÂn
1983; Braun and Hunt 1983; Ferguson and Sealy 1983; Horsfall 1984; Stamps et al. 1985; Gottlander 1987), as well as cases of parents actively promoting the death of last-hatched chicks by an uneven distribution of food (Drummond et al. 1986; Drummond and GarcõÂ a Chavelas 1989) or by infanticide (Newton 1978; Urrutia and Drummond 1990). The available information is still too scarce to correlate the appearance of these contrasting behaviours with other ecological features of the species (Drummond and GarcõÂ a Chavelas 1989; Forbes 1993; Nilsson 1995), but it is suggestive that two of the few bird species that show parental behaviours conducted to reduce sibling aggression are opportunist predators/carrion eaters. Quality of senior chicks Cainistic chicks had similar size and condition to senior chicks in multiple broods without mortality. Senior chicks in multiple broods were in better condition that single chicks surviving from multiple broods, and senior chicks in broods without mortality were larger and in better condition at ¯edging than senior chicks in broods where a chick starved. This result supports the basic idea from which Simmons' hypothesis was born: by killing its sibling early in the nestling period, a senior chicks avoids a risk of reaching ¯edging in poor condition. The condition of senior ¯edglings was aected by an interaction between year and mortality. In a year with high mortality by starvation and bad breeding conditions due to unfavourable weather and low availability of diseased rabbits (1988; see Fig. 4 and VinÄuela and Veiga 1992), senior chicks in nests where a chick starved attained a similar condition as those in nests without mortality. In contrast, 1987 was a good year for breeding during the whole nesting season, and 1989 was intermediate, with good conditions early in the season, but poorer conditions later (this explaining the smaller size and poorer condition of senior chicks in 1989; VinÄuela and Veiga 1992). This result suggests that two mechanisms to regulate productivity are simultaneously acting in this species, brood reduction and variation in growth rate or ®nal size. When conditions are especially poor, early brood reduction may allow parents to raise highquality senior chicks (1988). When conditions are better, brood reduction would be delayed, as the parents try to keep alive all the chicks by distributing resources, but at the cost of reduced growth rate or ®nal size (1987 and 1989). Rearing a higher number of chicks may have negative consequences on chick growth (e.g. Anderson 1990a), especially for later-hatched, but also for dominant chicks (Moreno et al. 1998). The strategy to prolong the life of all chicks, as well as a lower feeding rate in some broods (Table 5), would explain the large difference in size and condition between senior chicks in broods with or without mortality during good years.
43
Test of Simmons' hypothesis Simmons (1988) predicted that cainism should be frequent in saturated populations of facultatively siblicidal species. However, subadult territory occupancy would indicate population instability, and cainism should occur less frequently. Population instability could explain the low frequency of cainism during 1988, but the black kite population in 1989 can be considered saturated, because it reached one of the highest densities known for the species, and no additional population growth was detected in subsequent years. However, the lowest frequency of cainism was found in that year. I do not have any clear explanation for the higher frequency of cainism in 1987, but I have not considered in this work one of the main factors that may facilitate the occurrence of cainism, namely the frequency with which the female is absent from the nest (Newton 1977, 1979; Anderson 1990a). Perhaps during 1987, some factor, such as scarce food during the early nestling period or increased disturbance near the nests, induced longer or more frequent absences of the female, facilitating higher levels of sibling aggression. Simmons also predicted that under conditions of population instability, cainism should be more frequent in smaller broods. The opposite was found in the black kite. The higher frequency of cainism in three-chick broods may be explained simply by the higher hatching asynchrony of those clutches, because cainism was also more frequently observed in experimentally asynchronised broods. Simmons (1988) also proposed that under strong population pressure, the traits favouring the occurrence of cainism should be enhanced. However, I did not ®nd larger intraclutch egg size variation, longer hatching asynchronies, or longer laying intervals when the population of black kites approached saturation. Although I did not systematically record the frequency of aggressive interactions between neighbouring pairs, these clearly increased from 1987 to 1989. This could explain the reduction in clutch size from 1987 to 1989. But, since cainism was not higher in smaller clutches, this cannot be considered as evidence supporting Simmons' hypothesis. The results obtained in this population of black kites do not completely invalidate Simmons' hypothesis, because the black kite may not be an adequate species to test it. Black kites are semi-colonial raptors, rarely maintain feeding territories (but see VinÄuela et al. 1994), and may reach some of the highest nesting densities known for raptors. Simmons presented his hypothesis speci®cally to explain cainism in strongly territorial raptors, such as eagles, and he has shown recently interesting evidence in the Wahlberg's eagle supporting his ideas (Simmons 1993, 1997). However, my work shows that cainism may appear, at least at a low frequency, in a context dierent to that outlined by Simmons' hypothesis that, consequently, is not a universal explanation for the phenomenon. Following Newton (1977) and Sim-
mons (1991), there may be a continuum from raptor species where siblicide is mainly related to food-regulated brood reduction and parent-ospring con¯ict (facultatively siblicidal such as black kites), to species where siblicide may be more related to the high-quality chick demands proposed by Simmons. Acknowledgements I greatly thank all the people who helped me during ®eld work, especially Javier LoÂpez Redondo for his observations from the blinds. Jose Pablo Veiga provided helpful criticisms and suggestions during ®eld work and on previous drafts of the manuscript. This is a contribution to the Research Project PB87-0405 of the DireccioÂn General de InvestigacioÂn Cientõ ®ca y TeÂcnica. During this work I was supported by a predoctoral fellowship from P.F.P.I., Ministerio de EducacioÂn y Ciencia. During the ®nal analyses and writing, support was provided by a Fulbright Postdoctoral Fellowship at Yale University and by National Science Foundation grant no. IBN-9407349 to S.R. Beissinger. Comments by T. Amundsen, J.M. Aparicio, S.R. Beissinger, C.C. St. Clair, L.S. Forbes, J. Moreno, two anonymous referees and, especially, R.E. Simmons improved previous versions of the manuscript. I declare that all the manipulations included in this paper were done with the necessary permissions and comply with the Spanish laws on scienti®c research and nature conservation.
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Communicated by F. Trillmich
