Do white stork (Ciconia ciconia) parents exert control over food ...

Ethology Ecology & Evolution 20: 361-374, 2008

Do white stork (Ciconia ciconia) parents exert control over food distribution when feeding is indirect? S. Djerdali 1, F.S. Tortosa

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and S. Doumandji

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1

Département de Biologie, Université Farhat Abbes, Sétif 19000, Algérie Dpto. Zoología, Universidad de Córdoba, C1 Campus de Rabanales, 14041 Córdoba, Spain 4 Ecole Nationale Supérieure d’Agronomie, 16200 El Harrach, Algérie 2

Received 16 November 2007, accepted 19 May 2008

Intra-brood food distribution in altricial birds can strongly affect nestling competitive hierarchies and subsequent brood reduction. Food allocation patterns result from scramble competitions among the nestlings, various forms of parental favoritism, and/or agonistic interactions among nestlings. Food allocation is related to agonistic interactions among nestlings or to parental favouritism in non-aggressive species. Since white stork chicks are not aggressive and they do not receive direct feeding, parental infanticide has been proposed as an alternative mechanism to control brood reduction. The capacity of white stork parents to control food allocation was examined. We hypothesized that parents favour the senior chick by adjusting prey size to suit its ingestion capacity. We experimentally manipulated (Spain 1996 and Algeria 2004) nestling size by exchanging the senior chick for a larger one. After the exchange parents delivered longer and heavier prey items and they increased the total food amount delivered to the brood, which benefited not only the senior chick but also its smaller nestmate. We also discuss the effect of environmental conditions over brood reduction by comparing chick mortality, intrabrood weight asymmetries and fledging success in years with above (2003 and 2004) and below (2002) average rainfall in the area. We conclude that parents may control intra-brood food distribution which enables them to invest more in larger sibs but not (under favourable conditions) at the expense of junior chicks. key words:

3

white stork, brood reduction, food distribution, nestling competition.

Correspondence, Francisco Sánchez Tortosa (Fax: 957212002, E-mail: [email protected]).

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S. Djerdali, F.S. Tortosa and S. Doumandji

Introduction . . . . . . . Methods . . . . . . . . Results . . . . . . . . Chick mortality and breeding success Variation in nestlings asymmetries . Exchange experiment . . . . Discussion . . . . . . . Acknowledgements . . . . . References . . . . . . .

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Introduction

In unpredictable environments birds have to adjust their current brood to food availability. By laying too few eggs parents may unnecessarily reduce their offspring production, but laying too many eggs may produce low quality nestlings with poor survival. Lack (1947) proposed that parents favour competitive asymmetries by hatching asynchrony. In addition to manipulations of hatching interval (see Magrath 1990, Stoleson & Beissinger 1995 for a review), intraclutch egg size differences (Slagsvold et al. 1984) and egg hormone content (Schwabl 1996) have also been proposed to be related to pre-hatching parental regulatory mechanisms. In obligate siblicidal bird species, nestmate attack each other as hatchings and the junior chick typically survives only when the senior sib dies. In species with obligate brood reduction the second egg has been proposed to act as an insurance against the loss of the first laid egg (Cash & Evans 1986) or be the consequence of an evolutionary trend favouring the raising of a high-quality offspring (Simmons 1988, but see Forbes & Mock 1998). On the other hand, facultative brood reduction occurs in a scenario where food supply affects the chance of survival of junior chicks since food distribution over the brood is strongly affected by food availability. Competition for food among brood mates is ubiquitous and the way in which this competition occurs varies among species. Severe agonistic interactions have been well described in raptors (Viñuela 1999), egrets (Mock & Ploger 1987) and boobies (Drummond & García-Chavelas 1989) where older chicks aggressively prevent their younger sibs from being fed or directly kill them. A less dramatic mechanism is that of parental favouritism towards larger chicks in non-aggressive species, where parents might allocate food in direct proportion to the relative size of the chick as in passerines (Redondo & Castro 1992) or where parents simply do not turn toward the lesser chick when feeding as in the Magellanic penguins (Boersma 1991). Theoretically, in species where last-hatched eggs have both extra reproductive value and insurance reproductive value (Mock & Parker 1986), it is expected that the optimal time for delaying death of victims will be longer for the parents than for the senior chicks. However, there is much controversy about whether parents or offspring are primarily responsible for controlling the distribution of food resources (Royle et al. 2002). In most studies showing food distribution data, the older nestlings obtain more food than younger siblings, as has been found in egrets (Wer-

Parental feeding in white stork

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schul 1979, Ploger & Mock 1986), passerines (Bengtsson & Ryden 1983, Redondo & Castro 1992, Smiseth & Amundsen 2002), babblers (Ostreiher 1997), boobies (Drummond et al. 1986, Drummond & García-Chavelas 1989), raptors (Forbes 1991, Anderson et al. 1993) and terns (Bollinger 1994). However, parents may try to prevent brood reduction, as shown in the rednecked grebe where parents attacked especially the older chicks after their first two weeks of life, causing their competitive advantage to be gradually reversed (Klokowski 2001). It is difficult, however, to distinguish whether unequal feeding distribution among siblings is a consequence of parental preference, or variation in the nestmates’ ability to monopolize access to the feeder (Clutton-Brock 1991, Ploger & Modeiros 2004). The white stork is an altricial long-lived species with no aggressive behaviour among nestlings. Clutch size ranges from 1 to 7 eggs (average 4) and the number of chicks that leave the nest ranges from 1 to 4 (Del Hoyo et al. 1992). Hatching intervals increase with clutch size and vary from synchrony in clutches with two eggs to 2 days (range 1 to 3 days) in five egg clutches (Tortosa & Redondo 1992). Chicks are fed by both parents until they abandon the nest when they are 50-65 days old. Nestlings are initially fed with invertebrates such as earthworms, orthopterans or coleopterans (Barbraud & Barbraud 1997, Hadji 1998). Small vertebrates such as amphibian larva, small lizards and mammals are also progressively included as nestlings grow (Tortosa 1992). Parents deliver food by regurgitating onto the nest floor after the nestlings have gathered around the parent’s head. Therefore, food distribution is a classic ‘scramble competition’, related only to differences in the chick ability to eat as fast as possible. Moreover, parents do not exhibit any obvious preferential treatment toward certain chicks when delivering food (Kahl 1972). However it has been reported that brood reduction in the white stork was accelerated by direct parental attacks (Schüz 1984), which has been proposed as an adaptive parental manipulation of brood size, before substantial resources are committed to offspring (Haig 1990). Accordingly, parents might have two types of control over intrabrood food distribution, firstly by deciding the moment to start incubation (and thus determine initial competitive asymmetries through asynchronous hatching) and secondly, through parental infanticide of certain nestlings (Zielinski 2002). We studied the effects of an experimental manipulation of intrabrood body mass differences by increasing the size of the heavier chick. It is known that white stork parents increase delivered prey size as a function of brood age, which could be interpreted as a way to relax the difficulties derived from a specialist small prey diet to an all-sizes diet (Tortosa & Redondo 1992). We hypothesized that parents are sensitive to the size of the senior chick and we predicted an increase in delivered prey size when the size of the senior chick was experimentally increased. However by selecting a larger prey size parents might influence feeding distribution simply because senior chicks can ingest all prey sizes, while smaller nestlings often cannot handle the larger prey items. Therefore we also predicted that intrabrood food distribution will be affected in the experimental broods since the larger chick will take a larger fraction of the feeding.

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Methods Experimental design The experimental study was conducted at two different sites and dates: in Cordoba (Southern Spain) in 1996 and in Ain Azel (Northern Algeria) in 2004. In 1996 we manipulated the body mass of the heaviest chick in a sample of experimental broods in a white stork breeding colony in Southern Spain with the goal of exaggerating sibling size asymmetries within the species’ natural range. As food availability and prey type changed rapidly the experiment was carried out during the first 10 days of May to avoid any seasonal effect. The experiment was designed with 15 control and 15 experimental broods from clutches with four or five eggs that retained three nestlings after hatching. However natural brood reduction left only 16 suitable broods of which 7 were experimental and 9 were taken as control broods. In both control and experimental broods we exchanged the heaviest chick for one of similar (control) or double mass (experimental). Before the exchange, the average body mass of the lightest, middle and heaviest nestlings (C, B, A chick hereafter) were (means ± SD) 281 ± 45 g, 398 ± 75 g and 411 ± 55 g respectively and they were 11 ± 2.6 SD days old. In the experimental broods A-chicks were replaced by chicks weighing roughly double the mass (975 ± 152 g, 17 ± 5.2 SD days old for the first hatched chick). In control broods A-chicks were replaced by chicks of similar mass (less than 50 g differences), giving a body mass after the exchange 251 ± 39 g, 371 ± 79 g and 480 ± 85 g for C, B and A chicks respectively. A-chicks removed from the experimental broods were placed in other broods of similar mass during the experiment. To collect feeding data, all chicks were fitted with a neck ring that prevented oesophageal food from passing to the stomach. After a parent delivered a meal, we induced the collared chicks to regurgitate. The days before and after the exchange we recorded the weight, length, number and type of prey in each chick’s oesophagus above the collar during two feedings early in the morning (8-10 hr). After recording data the collar was removed, allowing the chicks to eat the prey. Due to the small sample size in 1996 that arose because of the difficulty to find appropriate broods for the exchange experiment in this species (same area, same date, similar clutch size, same brood size) we decided to repeat the exchange experiment in 2004 in the Algerian colonies following the same protocol described above. However, in 1996 we did not find any effect of the exchange alone and the only significant effect was due to the presence of a larger chick (see results), therefore in 2004 we used all the available broods (n = 11) as experimental broods for the exchange experiment. As in 1996 these broods had three nestlings coming from clutches with four or five eggs. Nestlings had a body mass of 231 ± 98 g, 368 ± 65g and 451 ± 81g for C, B and A chicks respectively and they were aged 12 ± 3.7 days (age of the first hatched chick). Exchanged A-chicks weighed 1066 ± 110 g. Again, A-chicks from the experimental broods were placed in other broods of similar mass during the experiment. The laying period extended from 6th March to 2nd May. To avoid any seasonal effect, exchange experiments were conducted during the first 2 weeks of May . In every case the exchanged chicks came from nearby broods and after the experiment all chicks were returned to their original nests. White stork parents immediately accept and feed any chick in the nest and nestlings transferred to foreign nests show a normal growth pattern after being transferred (Tortosa & Redondo 1992).

Observational breeding parameters We recorded mortality and breeding success in the Algerian breeding colony in 34, 35 and 40 broods during 2002, 2003 and 2004 respectively. To determine hatch-


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ing order, nests were visited every 3rd day and chicks were individually marked. After hatching broods were monitored weekly. When a dead chick was still in the nest we determined the age of death according to the condition of the body. If the body was not in the nest we assigned age of mortality as the midpoint from the last visit. To calculate fledging success we only took into account those nests where at least one egg hatched. Fledging success was defined as the number of chicks that complete their growth and left the nest. Average rainfall during the period 1983-2005 was 276 mm. Rainfall during study years was 186 mm (2002), 339 mm (2003) and 430 mm (2004). Intrabrood body mass differences were measured with an asymmetry value (Bryant 1978) calculated as: (mass of the heaviest chick) – (mass of the lightest chick) / mean mass of the brood. The asymmetry index was calculated in 26, 33 and 13 broods in 2002, 2003 and 2004 respectively. In these broods the nestlings’ body mass was recorded every 5th day on average (range 4-6 days) from hatching to fledging. The maximum asymmetry index in every year was calculated as the mean value for the highest record of this parameter in each brood. All variables were normally distributed, except for age of death which was normalized by a log transformation. To check for the effect of the exchange experiment and the body mass rank of the nestlings on the individual food intake (heavier rank = 1, intermediate rank = 2, lighter rank = 3) we performed a factorial nested ANOVA with rank and experiment (nestling exchange) as factors and nest as a random factor to avoid pseudoreplication. Results are presented as mean + SD.

Results

Chick mortality and breeding success In non-manipulated broods in Algerian colonies, brood reduction occurred earlier in 2002 (mean age of death 7.8 ± 5.9 days) than in 2003 (18.6 ± 13.5) or 2004 (13.9 ± 9.1) (ANOVA, F(2,127) = 14.1, P < 0.001); the latter two were similar to each other (Tukey post hoc test P > 0.05). As well, most 2002 victims died early from starvation (during the first 2 weeks) whereas in 2003 and 2004 some junior chicks did not die before their 40th day (Fig. 1). Mortality was related to hatching order during the 3 years of study with a higher mortality rate in those chicks hatching later (Table 1). In 2002 all 4th or 5th chicks died and only 50% of first hatched chicks survived until fledging. Fledging success in 2002 (0.91 ± 0.17 chicks per nest) was less than half that of 2003 (2.4 ± 0.18) and 2004 (2.3 ± 0.12) (ANOVA, F(2,109) = 25.5, P < 0.001; there were no differences between the latter two, Tuckey’s post hoc P > 0.05). Variation in nestlings asymmetries Intrabrood body mass differences increased after hatching and tended to peak during the second or 3rd week after hatching (Fig. 2). When we selected the higher asymmetry value in every brood the yearly mean values were 0.52 ± 0.34, 0.74 ± 0.29 and 1.03 ± 0.19 in 2002, 2003 and 2004 respectively (ANOVA F(2,70) = 13.6, P < 0.001) and differed across all 3 years (Tukey tests,

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1XPEHURIFDVHV

Age at dHDWKGD\V Fig. 1. — Number of deaths at different ages in 2002, 2003 and 2004.

)LJ Table 1. Percentage of surviving chicks depending on hatching order during 2002, 2003 and 2004. Hatching order 1 2 3 4 5

2002 (34 clutches)

2003 (35 clutches)

2004 (40 clutches)

50 35 28 0 0

92 84 50 28 14

100 93 38 16 0

all P < 0.05). Broods reached their maximum size asymmetry index more rapidly in 2002 (at age 8.3 ± 1.4 days), than in 2003 (12.5 ± 1.3 days) or 2004 (14.5 ± 1.9 days) (ANOVA F(2,70) = 4.1, P = 0.02), with 2002 differing from the other 2 years, which were similar. In 2002, with a higher mortality rate, asymmetries declined earlier since brood reduction occurred during the first 10 days and the deaths of the smaller nestlings reduced total asymmetries among the remaining chicks. In 2003 and 2004 the lower and delayed mortality of nestlings maintained higher asymmetries in the brood since junior chicks died later or survived until fledging.


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1.6 2002 2003 2004

1.4 1.2

Asymmetry Index

1.0 0.8 0.6 0.4 0.2 0.0 0.2

0

5

10

15

20

25

30

35

40

45

50

55

60

65

70

Age (days)

Fig. 2. — Variation of the intrabrood body mass Asymmetry Index (see Methods) during the nestling periods of 2002 (close symbols), 2003 (open triangle) and 2004 (open circles).

Fig. 2

Exchange experiment Data from Southern Spain1996. Control broods did not show significant differences on individual food intake before and after the exchange (F (1,8) = 0.22, P = 0.91). The opposite was found in the experimental broods (F(1,6) = 17.6, P = 0.001) (Fig. 3). Rank order had a significant effect on individual food intake in both control (F(2,16) = 145, P = 0.001) and experimental broods (F(2,12) = 20.7, P = 0.001) broods. The interaction between order and treatment was not significant in control broods but the opposite was true in experimental nests (F(2,12 ) = 3.2, P = 0.05). Parents increased both the mean prey size and the total mass of prey delivered after the senior chick was replaced by a larger nestling. Specifically, mean prey weight tripled after the exchange (Table 2). Data from Algeria 2004. As found in 1996, in 2004 the white stork parents from experimental broods also increased the prey size and the total prey mass delivered to the brood (Table 2). Experimental exchange had a significant effect on individual food intake (F(1,10) = 5.2, P = 0.003), that is parents increased the food delivered to the brood after the exchange. The allocation was more skewed because the heavier chick consumed disproportionately more than its brood mates (F(2,20) = 11.2, P = 0.001). The interaction between treatment and rank was also significant (F(2,20) = 3.3, P = 0.05) since the senior chicks ate a higher relative amount of food after the exchange (Fig. 3).

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Table 2. Effects of exchange experiment on prey eaten by chicks in control (Cont) and experimental (Exper) broods in 1996 and 2004. Total weight is the sum of the weight of the prey eaten by every chick. Means + SD. Year Mean prey length Exper 2004 Cont 1996 Exper 1996 Mean prey weight Exper 2004 Cont 1996 Exper 1996 Total weight Exper 2004 Cont 1996 Exper 1996

Before exchange

After exchange

Paired t-test

5.2 ± 2.5 cm 6.4 ± 1.2 cm 5.8 ± 2.1 cm

7.4 ± 4.4 cm 5.5 ± 1.4 cm 9.7 ± 6.5 cm

t(10) = 2.3, P = 0.041 t(8) = 0.47, P = 0.46 t(6) = 2, P = 0.04

2.7 ± 1.8 g 7.5 ± 2.5 g 6.8 ± 5.2 g

10 ± 12.5 g 8.1 ± 5.2 g 20.3 ± 16 g

t(10) = 1.97, P = 0.07 t(8) = 0.67 P = 0.51 t(6) = 2.8, P = 0.03

30.8 ± 14.6 g 42.7 ± 33.4 g 39.2 ± 31 g

64 ± 24.7 g 41.1 ± 76 g 61.2 ± 25 g

t(10) = 3.9 P = 0.002 t(8) = 0.8, P = 0.31 t(6) = 3.7, P = 0.001

Discussion

Empirical field data show that a correlation exists between chick mass and their subsequent survival (Magrath 1991, Gaston 1997, but see Amundsen & Slagsvold 1998). Therefore, if the quality of an individual during its nestling stage might influence its future parental lifetime we would expect that parents may have some control over food allocation in the brood. The handicap imposed on junior chicks by hatching asynchrony easily explains early starvation of the last hatched nestlings under poor environmental circumstances minimizing the cost of brood reduction. Conversely, when food is abundant parents might keep their options open by letting marginal offspring overcome the handicap of hatching last. In species with agonistic interactions among nest mates an aggressive dominance hierarchy is established and food distribution is related to the chicks status (Drummond et al. 1986, Anderson 1991). When no direct aggressive interactions exist among the nestlings, as appears to be the case in passerines, nestling rank appears to be a better predictor of food distribution and parents commonly show a stronger preference for seniors not only by nestling behaviour but also by parental preferences for seniors based on non-signaling cues, such as body size (Smiseth et al. 2003). As no aggressive dominance exists in the white stork (Redondo et al. 1995) and parents do not feed individual nestlings, the control over brood reduction should be related only to the hatching pattern. However, our results show that white stork parents seem to exert some control over food allocation by selecting prey size. In our experiments parents increased mean prey size, which favoured the largest chick but not at the expense of the smallest one. Exchange experiments were conducted in good years since in the Mediterra-

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Fig. 3. — Food intake (g ± SD) of every nestling in the brood before and after the exchange of the heaviest chick for a similar weight chick (control) or for a heavier chick (experimental) in 1996 and 2004. Rank order = 1 for the heavier chick in the brood.

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nean region rainfall is a constraint and there is a positive correlation between rainfall and breeding success in the white stork (Mouali-Grine et al. 2004). However some chicks die of hypothermia during periods of hard rain before they develop their thermoregulation abilities when they are about 3 weeks old (Tortosa & Castro 2003). In 1996 when we conducted the experiments in Southern Spain rainfall was 530 mm in the study area, a good year since the average precipitation for the period 1984-2004 was 390 mm in this area. In 2004 when the same experiment was conducted in Algeria the rainfall in the study area was 430 mm, also a good year when compared to the 275 mm on average from the period 1983-2005 (C.M.S. 2005). Under these favourable conditions parents may increase food allocation to the larger chicks while still keeping open the option of increasing their breeding success with marginal chicks because, given good environmental conditions, marginal offspring can successfully overcome the handicap of hatching last (Royle 2000). In good years white storks might increase their breeding success by providing enough food for both the senior and last hatched sibs. During these good years our data show higher and later intrabrood asymmetries as a consequence of the relative faster growth of the senior chick while the junior is still alive. Junior chicks growing at a slow rate finally reach a similar body mass as seniors and thus the asymmetries decrease at the end of the rearing period. It is known that white stork chicks show a great capacity to recover after a period of food shortage since starving last hatched nestlings recovered weight and reached a normal asymptotic mass when they received enough food after being transferred to one chick broods (Tortosa & Redondo 1992). Reports on the selective feeding of smaller chicks are scarce, although in some species parents appear to control food distribution among the young, when food is abundant, by selectively feeding junior chicks (Stamps et al. 1985, Gottlander 1987) or delivering larger loads of food to broods with large size asymmetries to ensure that small chicks are fed (Krebs et al. 1999). Our results support resource allocation theory (Forbes 1993, Mock & Parker 1997) since the brood hierarchy would ensure that junior chicks only receive resources after the needs of senior sibs have been satisfied. Our results also agree with the hierarchy model (Parker et al. 1989) or the despotic allocation model (Forbes 1993) that propose a cascade type of intrabrood resource allocation: once the needs of core sibs are satisfied, marginal nestlings receive the remaining food without any detrimental effects on core brood members. This was also suggested by Forbes & Glassey (2000) who found that the presence of the marginal offspring had little effect upon the growth of core nestlings. According to parental investment theory breeding adults should adjust their investment to maximize future net benefits (Trivers 1972, Maynard Smith 1977) by providing more for older, larger or higher-quality offspring (Carslisle 1985, Redondo 1989). To favour bigger chicks parents could keep their effort constant by selectively feeding senior nestlings at the expense of the junior or alternatively they could increase their foraging effort. If parental effort increases this could benefit only senior chicks by holding constant the food to junior chicks or, as a second option, junior chicks could also benefit from the extra food delivered by parents. Our results show that experimental white stork parents with a larger senior chick, in addition to increasing food


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provisioning to the senior chick, also increased the total food delivered to the brood. The white stork is a long lived species and therefore parents might act in a prudent way since parental investment theory predicts that if parents increase the effort they put into the current brood, the additional investment would be made at the expense of future sibs (Drent & Dann 1980). According to this strategy white stork parents have been found to favour their own survival against the number of chicks (Sasvari & Hergyi 2001). However, a high value current brood could stimulate parents to invest more. Evidence of a higher parental effort being given to more valuable broods has been shown in other bird species. Great tit parents appear to be able to adjust their nest defense behaviour to the expected fitness value of their offspring (Ryntkönen 2002). In the same way, female mallards adjust parental care according to the expected benefits of current offspring by fine-tuning their level of parental care according to the increased prospects for offspring survival as they age (Ackerman & Eadie 2003). In our experiment, we increased the size of the older nestlings which might have produced a positive stimulus to the parents due to the higher value of their “new” brood. If parents are positively size-sensitive, nestlings might benefit by installing themselves in the nests of younger neighbouring broods. Nest switching is known to occur in the white stork nestlings that abandon their natal nest prior to independence in dense breeding colonies (Redondo et al. 1995). Chicks that abandon their brood move into nests containing fewer and younger nestlings where they increase their food intake compared to their natal broods. Redondo et al. (1995) showed that foster parents tend to increase their feeding effort after receiving a larger extra chick as also found in the present work. When foster parents adopt a nestling they find a new situation with both a larger brood and chick. To adjust food deliveries to brood size is a widespread pattern in birds (Ploger 1997) as also found in the white stork that increases its feeding effort in larger broods (Tortosa & Redondo 1992). Therefore parental feeding effort seem to be sensitive to both brood and chick size. Since white stork chicks are not aggressive and senior chicks cannot monopolize food by directly interfering with food allocation by parents to individual nestlings, it has been suggested that the process of elimination of the weakest chick in the white stork is very ineffective and this in turn has favoured parental infanticide as a way to eliminate the surplus chick themselves (Zielinski 2002). However, our results suggest that lack of monopolization may be actually a direct consequence of parental control over brood reduction because parents feed larger prey to larger nestlings, which may disadvantage juniors when there are food shortages, but did not lead to monopolization by seniors in this year of good environmental conditions. We conclude that white stork parents may maintain a level of control over food distribution and subsequent brood reduction despite using indirect methods of feeding nestlings. The increasing relative food intake by the senior chick did not affect their nest mates and therefore this is not a case of favouritism, at least not in good environmental circumstances. However we predict that in a food shortage period white stork parents would also optimize their foraging effort by selecting larger prey due to the lower cost of feeding on them what may passively stimulate brood reduction (Tortosa & Redondo 1992).

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Acknowledgements We thank Douglas Mock and Bonnie Ploger for their valuable comments on the manuscript and their help with the English language. Sophia Djerdali was supported with a pre-doctoral grant from the Algerian Ministère de L’Enseignement Supérieur et la Recherche Scientifique. The experiments were conducted according to the current Algerian and Spanish laws.

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