Experimental Manipulation of Brood Reduction and Parental Care in Cooperatively Breeding White-Winged Choughs

Experimental Manipulation of Brood Reduction and Parental Care in Cooperatively BreedingWhite-Winged ChoughsAuthor(s): Christopher R.J. Boland, Robert Heinsohn and Andrew CockburnSource: Journal of Animal Ecology, Vol. 66, No. 5 (Sep., 1997), pp. 683-691Published by: British Ecological SocietyStable URL: http://www.jstor.org/stable/5921 .

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Journal of Animal

Ecology 1997, 66, 683-691

Experimental manipulation of brood reduction and parental care in cooperatively breeding white-winged choughs CHRISTOPHER R.J. BOLAND, ROBERT HEINSOHN and ANDREW COCKBURN* Evolutionary Ecology Group, Division of Botany and Zoology, Australian National University, Canberra ACT 0200 Australia

Summary

1. White-winged choughs, Corcorax melanorhamphos (Vieillot), are obligate cooperative breeders. Only very large groups routinely fledge all their brood of three to four chicks, while small groups usually lose young during the nestling period. Hatching asynchrony generates a weight hierarchy within the brood, and small, late-hatched chicks are most susceptible to mortality. 2. In order to examine the effects of food availability on parental care and brood

reduction, we provided supplementary food to groups during late incubation and the

nestling phase. 3. Food supplementation increased the rate of food delivery to the nest by both breeders and helpers, leading to increased chick survival and fledging, and reduced variance in chick size at fledging. Helpers with supplemental food appeared more

responsive to the need of chicks, increasing food delivery rates as the chicks grew older, and as brood size increased. 4. Control groups fed larger chicks preferentially, while supplemented groups favoured small chicks. This suggests that choughs deliberately manipulate the survival of individual young to maximize the fledging of healthy chicks, consistent with Lack's

hypothesis for hatching asynchrony. 5. These data support the hypothesis that choughs must breed in groups because they cannot provide enough food to nestlings without help. Hatching asynchrony and behavioural control over brood reduction allow choughs to maximize offspring pro- duction according to group size and food availability.

Key-words: brood reduction, cooperative breeding, Corcorax melanorhamphos, food

supplementation experiments, hatching asynchrony.

Journal of Animal Ecology (1997) 66, 683-691

Introduction

The 'skills hypothesis' for cooperative breeding suggests that helping is a reflection of slow acquisition of foraging skills, preventing independent breeding by young birds (Lack 1954, 1968). This hypothesis receives most support from data on white-winged choughs (Corcorax melanorhamphos) where: young acquire foraging skills very slowly (Heinsohn, Cock- burn & Cunningham 1988; Heinsohn 1991a); helping is contingent on the availability of food (Cullen, Hein- sohn & Cockburn 1996); and helpers suffer energetic

? 1997 British Ecological Society * Correspondence author.

costs when they provide help in some circumstances (Heinsohn & Cockburn 1994). Unassisted pairs cannot breed successfully, and reproductive success increases linearly with group size across the entire range of group sizes for which data are available (2- 15 birds; Rowley 1978; Heinsohn 1991b). Despite this large body of evidence that cooperative breeding is closely linked to foraging ability, conclusions remain based on correlation rather than experiment. In this study, we report the effects of food supplementation on reproductive success.

As with many other birds, the proximate cause of nestling mortality in white-winged choughs appears to be modulated via hatching asynchrony. Choughs

683



incubate their clutches as soon as the first egg is laid, and eggs invariably hatch a day or more apart, causing a weight hierarchy within the brood (see full descrip- tion by Heinsohn 1995). Many hypotheses have been

suggested to account for hatching asynchrony (reviewed by Magrath 1990; Stenning 1996). Lack's brood reduction hypothesis has been most influential

(Lack 1954, 1968; Ricklefs 1965). Lack (1954) suggested that parents are 'optimistic' and produce more

young than they can usually rear in order to be able to

exploit any surge in food resources. They use hatching asynchrony to create expendable offspring when food

supply proves poor. Fatal levels of sibling competition reduce brood size to an appropriate level for the parents if suboptimal resources prevail. The later-hatched

offspring, which have obtained the least parental investment, die first. The hypothesis relies on the

assumption that first-born siblings, being slightly larger, maintain their advantages through superior competitiveness. Observational studies suggest that this assumption is valid; older, larger nestlings are able to outposition smaller siblings, raise their gapes higher and vocalize louder (Magrath 1990). Con-

versely, brood reduction should not occur if food

proves plentiful (but see Amundsen & Stokland 1988; Skagen 1988; Wiebe & Bortolotti 1995). Thus, the maximum clutch size should approximate optimal brood size given the most favourable conditions. It is assumed that if eggs were to hatch synchronously, food shortage could lead to poor growth of all nest-

lings and cause complete brood loss by starvation.

Consequently, the ultimate effect of hatching asynchrony is to maximize brood size in the face of unpre- dictable conditions. By contrast, Nilsson (1995) suggests that such evidence most frequently indicates

parent-offspring conflict over brood size, with the conflict resolved most often in favour of the young that outcompete their nestmates.

To date, there have been very few experimental studies designed to test the brood reduction hypothesis, and these have produced mixed results. Magrath (1989) manipulated the clutches of blackbirds while

altering food availability. As predicted by the hypothesis, asynchronous broods fledged significantly more

young compared to synchronous broods in poor conditions. In contrast, in favourable conditions, there was no significant difference in the reproductive success of synchronous and asynchronous broods. How- ever, similar experiments in other species have not

consistently demonstrated equivalent effects (Skagen 1988; Wiebe & Bortolotti 1995).

There are several testable predictions of the brood- reduction hypothesis which include: (i) chicks should die in reverse order of their position in the brood hierarchy (that is, youngest first); (ii) most chicks that die should do so quickly, thereby reducing wasted

parental investment; (iii) brood reduction should allow parents to devote energy to an optimal brood size so that the remaining chicks are fledged in good

condition; (iv) the degree of brood reduction should track the available resources (Temme & Charnov

1987). The hypothesis can be extended to suggest that:

(v) if food is frequently scarce, parents that actively reduce brood size by destroying the smallest young will be favoured; and (vi) when food is abundant, parents should employ behavioural traits to allocate food resources selectively to youngest hatchlings in order to overcome the competitive asymmetry of the brood.

This study investigates the predictions of the brood- reduction hypothesis by artificially altering environ- mental conditions during the breeding season of

groups of choughs. The conflict between the needs of the young and the ability of feeders is of special interest because of the importance of helpers at the nest in this species (see also Dyer & Fry 1980; Lessells &

Avery 1989).

Methods

STUDY AREA

Observations on the nesting attempts of groups of

white-winged choughs were made during the 1995/96 breeding season (August to February). Groups were located on the lower slopes of Mt Ainslie and Black Mountain, Australian Capital Territory, 36?05'S, 149?15'E. The vegetation at all sites is eucalypt wood- land dominated by Eucalyptus mannifera, E. rossii and E. macrorhyncha.

The nesting attempts of 26 groups ranging in size from four to 11 members (mean size = 6-2 + 2-1 SD) were observed intensively. Once a nest was found, clutch sizes and hatching dates were obtained using a mirror attached to a telescopic pole. The fate of each clutch was checked daily until the nest fledged or failed. The groups included 165 adult choughs. Sixty- three birds (38%) in the study had been colour- banded, and all birds could be grouped into four distinct age classes (1, 2, 3 and 4+ years) according to

slight variations in eye colour (Rowley 1975). Choughs reach sexual maturity at 4 years (Rowley 1978).

EXPERIMENTAL METHODS

Groups were divided into two categories, 'experimental' and 'control'. An attempt was made to pair experimental and control groups according to group size and date in the breeding season. Thus when a

group of a particular size initiated breeding, it was

randomly assigned to the experimental or control cat-

egory, with the next group of comparable size to initiate breeding assigned the opposite condition (Table 1). Experimental groups received additional food supplies every morning and late afternoon from the period prior to hatching until the young fledged (approximately 6 weeks). Supplementary food was

684 Brood reduction in

cooperatively breeding choughs

? 1997 British Ecological Society Journal of Animal Ecology, 66, 683-691



Table 1. The number of control and experimental groups of white-winged choughs for each group size

Group size Control Experimental

4 3 4 5 2 2 6 2 2 7 2 1 8 2 2 9 1

10 0 1 11 1 0

Total 13 13

temporarily elevated the number of food returns to the nest.

Because choughs build conspicuous nests and habituate well to observers, it was possible to observe

feeding of individual nestlings. Throughout the obser- vation periods the timing of each visit to the nest

by group members was recorded, noting the age and

identity of the bird, whether or not two or more birds fed young simultaneously, which nestlings received the food, the number and type of food items returned and whether or not the feeder relieved the previous brooder.

STATISTICAL MODELLING

placed upon a 'feeding tray' located within 20m of the base of the nesting tree of each experimental group. The additional food comprised 1 kg of shred- ded cheese mixed with an amino acid powder especially formulated for birds ('Powell's meat meal'; 55% protein), and was readily consumed by the

choughs.

DATA COLLECTION

Data were collected from 21 August 1995 to 4 Feb-

ruary 1996. Nests were reached by a single-rope climb-

ing technique or by using a trailer-mounted cherry- picker. The tendency for choughs to build their nests

upon thin branches meant that it was not possible to climb to the nest of certain groups. The weights of

nestlings from 16 groups (nine fed, seven unfed) were measured at 10 and 20 days after the first egg hatched and on the day of fledging. The fledglings, which cannot fly for about a week after they leave the nest, were

caught by hand. To enable recognition of individual

nestlings from the ground, nestlings were daubed with nontoxic acrylic paint on the throat and back of the head (see Heinsohn 1995). The order of colours

(orange, green and white) within broods was randomized to eliminate potential colour effects. In order to establish timing of death of individual nestlings for each group the number of chicks in each nest was checked daily.

Each nest was observed for continuous periods of 60 Inin on seven occasions at 4-day intervals following the hatching of the first young. In order to minimize

any possible effects of disturbance, nest watches were

always preceded by an habituation period of 20 min

(or occasionally more if deemed necessary from the behaviour of the group). The nest was observed from around 20 m using binoculars so as to minimize disturbance to the group while still permitting individuals at the nest to be aged and identified with confidence. The time of day of each nest watch was randomized to avoid potential bias caused by any daily changes in

activity. Nest watches never occurred within 90 min of supplementary feeding episodes, as feeding often

Data were analysed using generalized linear models

(Aitkin et al. 1989). Survival data were analysed using Cox's proportional hazards model as implemented in JMP v. 3 (SAS Institute 1994). Conventional least

squares models were fitted in other cases, often after the data had been transformed to ensure that the residuals had a normal distribution. In all figures we

present the untransformed data and back-transformed model predictions. The data were often in the form of mixed models, where, in addition to the fixed

explanatory variables of interest, sampling involved

replication across an additional random variable (the group to which the bird belonged, or the nest at which the group was fed; Bennington & Thayne 1994). In all mixed model analyses presented here, sample sizes varied for both random and fixed variables, so it was

inappropriate to use least squares methods to estimate the importance of the explanatory variables. Accord-

ingly, the restricted maximum likelihood (REML) procedure available in GENSTAT v. 5-3 (GENSTAT 5 Committee 1993) was used, in which 'group' or 'nest' was treated as the random factor.

In all analyses, we initially fitted full models con-

taining a set of explanatory variables and for cat-

egorical variables, interaction terms. Nonsignificant terms were progressively discarded to derive a par- simonious model containing only significant (P < 0-05) terms or interactions.

Results

PROVISIONING RATES

Throughout nesting attempts, groups of choughs for-

aged on invertebrates obtained from the soil surface or by digging. Over the course of the study we observed 1918 nest visits resulting in 3063 food items being delivered to the chicks. Choughs in experimental groups consumed very large quantities of cheese. Indi- viduals would often fly directly to the feeding station immediately after being relieved of brooding at the nest. It was not unusual for individuals to consume over 30 pieces of cheese in succession, before joining the remainder of the group to forage on natural items.

685 C.R.J. Boland, R. Heinsohn & A. Cockburn




However, they brought relatively little cheese to the

nest; only 6-5% of all food items brought to the nest were taken from the feeding station. The food sup- plement subsidized the intake of natural food items, which are presumably more difficult to obtain.

Groups differed in age composition. We estimated for both control and experimental groups the relative investment expected according to the age classes present in those groups. In control groups, contributions increased linearly with age (Fig. 1: X2 = 27-9, d.f. = 3, P < 0-001). In contrast, in experimental groups one-

year-old choughs provisioned food at a rate less than

expected (Fig. 1: x2 = 11.1, d.f. = 3, P < 0.05). All other individuals provisioned at about the expected rate. The workload of all group members increased as food became more available.

Provisioning rates were log-transformed to nor- malize the residuals, and analysed using the REML

procedure. Initial models contained laying date (early, intermediate, late) and experimental condition (fed, control), which were treated as factors, and chick age and group size, which were treated as continuous vari-

ates, and all possible interaction terms. Exploratory analysis suggested that it was most appropriate to log- transform chick age. All interaction terms and the term for laying date were discarded (all P > 0.05), although there was a tendency for experimental condition to interact with brood size (X2 = 3 6, d.f. = 1, P 0 0-06). The significant terms remaining were log of chick age (Fig. 2a: change in deviance estimated via

REML; x2 = 160.6, d.f. = 1, P < 0-0001), group size

(Fig. 2b: x2 = 42-4, d.f. = 7, P < 0-001), and experimental condition (Fig. 2: x2 = 611.1, d.f. = 1, P <

0-0001). Feeds increased with chick age and group

U) (n 0 0

0 a 0

a a 0 a)

a 'a x a, 0

a, U, .0 0

41

Z: LL

+1

(I)

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0-4

0-2


1 2 3 4+

Age class (years) Fig. 1. The proportional contribution of food delivered to white-winged chough nestlings as a function of age of the oldest chick for unfed groups (unshaded bars) and fed groups (shaded bars). Age classes provisioning at rates greater than 1 deliver more food than would be expected if all birds of all age classes contributed equally. The small number of one- year-olds in the sample reflects poor breeding during a severe drought in 1994. Figures represent the number of birds in each age class.

50 8

(a)

LL CI) +1 0 0

L-

0, (1)

Uf) a

'F TT

40 - 13 13

I l 1 1 30 - 13

13 13

Fed

20 -

10 - 10 -

4 1-11 1 / 10 12 1 C

1 1 o a- ? t - Control

0 4 8 12 16 20 24 28

Age of oldest chick (days)

50

(b) 40

+1 3 30 0 .r .- a)

00 0- 20

0

i 1

13

I 1

7

7

14 6 14 25 Fed

I

9 6 6 12 13 13 a 9 12

Control I I I I

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4 6 8 10

Number of birds in group

12

50

40 - (C)

30 -

I

18

Fed

21 44

I I

20 -

10 Control

4 40 16 8 I i I I

1 2 3 4

Number of chicks in brood i Fig. 2. The effects on the food provisioning rates (+ SE) to white-winged chough nestlings of (a) food supplementation and age of the oldest nestling; (b) group size and food supplementation; and (c) brood size and food supplementation. Experimental groups are denoted by 0 and control group by O. Lines depict predictions from the REML model. These predictions represent back-transformations from the original model which was calculated for log-transformed data, and control for the effects of the variables not represented in each graph (in Fig. 2a, estimates include brood size and group size effects, as well as controlling for the identity of the group).



I I I I I I



size, and were dramatically enhanced by providing supplementary food. If the interaction term is included in the model, experimental groups increased their workload with increasing brood size, but any increase in control groups was slight or nonexistent

(Fig. 2c).

SURVIVAL OF YOUNG

The cause and timing of death of each nestling was recorded. Two nestlings were probably killed by aerial

predators. One was found decapitated at the base of the nest tree, while the second nestling showed no evidence of starvation; it was not emaciated prior to

death, nor was it excluded from food (cf. Mock 1994). Indeed, it was the oldest and largest chick in the brood and was frequently fed during the previous nest watch

(3 days previously). In all other brood losses the youngest, smallest nestling died first (n = 23).

Chick mortality was reduced by the provisioning of food. The hazard of mortality of fed chicks was 45% of that observed for control chicks (26% and 73% are 95% confidence intervals; proportional hazards

model; 2 = 11-2, d.f. = 1, P < 0-001). Chick mor-

tality was also lower in large groups (six or more birds) relative to smaller groups; 63% (41%, 96%) (Z2 = 4-5, d.f. = 1, P = 0-03). There was no interaction between

group size and experimental condition (X2 = 0.8, d.f. = 1). Brood reduction in control groups occurred in two distinct phases: a rapid, early phase in which about 30% of nestlings died within the first few days of hatching; this was followed by a gradual loss of the surviving nestlings (Fig. 3). In all, 47% (20/43) of control nestlings failed to fledge. No nestlings died after day 21 (Fig. 3). In contrast, experimental groups lost only five nestlings (13%), two of which were probably the victims of predation. No nestlings died from starvation after day 13 in experimental groups (Fig. 3). Thus, nestling mortality was almost eliminated from

0.9

a,

ca

0

0. 0-

0-

08

0-7

06

'lb

\>o

Control \oo o? ooo 0-5

0

( 1997 British Ecological Society Journal of Animal Ecology, 66, 683-691

5 10 15 20 25 30

Age of chick (days) Fig. 3. Proportion of white-winged chough chicks surviving to particular ages in experimental (O; initial sample size = 38) and control groups (0; n = 43).

4-0 -

3-5 -

In

a, 0) -a3

a, .0

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3-0 - Fed

* * X

2-5 -

2-0 -

1-5

1.0 0

Co o

Control

0-5

(nn

2 4 6 8 10 12

Number of birds in group Fig. 4. Reproductive success in white-winged choughs as a function of group size and experimental condition (O denote control groups; 0 denote fed groups). The initial brood size was always three or four hatchlings. Lines represent predictions from the analysis of covariance.

groups with greater food availability. As a conse-

quence, the reproductive success of groups increased

linearly with group size (Fig. 4: ANOVA; F\123 = 9.4, P < 0-001), and increased with additional food (Fig. 4:

ANOVA; F1,23 = 10.8, P < 0-001).

WEIGHT OF YOUNG

The absolute weights of young in control and experimental groups were compared using the REML procedure. There was no effect of laying date (treated as a factor because of the obvious nonlinearity in growth rates), group size (treated as a variate), or any interactions which included these terms on the weights of chicks (all P > 0-05). There were significant interactions between age of chick (treated as a factor) and hatch order (treated as a continuous variate; Z2 = 7-2, d.f. = 2, P < 0.05), between experimental condition and hatch order (X2 = 12-3, d.f. = 1, P < 0-001), and between experimental condition and age of the chick

(X2 = 15-2, d.f. = 2, P < 0-001). The three-way interaction term between these variables was not significant. (X2 = 42, d.f. = 2). Size hierarchies were

initially evident for both experimental and control

broods, but as chicks grew, the size hierarchies in

experimental broods were much reduced (Fig. 5). Offspring in groups which suffered early brood

reduction (prior to day 10) benefited from higher mean

fledgling weights than groups which reduced late or not at all (mean weight 'early' = 263-2 + 6-6 g, n = 9

broods; 'late' = 242-5 + 5.3, n = 14 broods; ANOVA, F1,20 = 6-04, P = 0-023). Thus, groups which experi- enced early brood reduction fledged less young, but those that did fledge were in better physical condition.

ALLOCATION OF FOOD TO INDIVIDUAL

YOUNG

Comparing the absolute weight of a chick with those of chicks from other nests does not indicate its 'intra-


0





U C/) +1

c-)

0) .5

300 -

0

250 -

200 -

150

100

6

9

6 \ 1

7\1

20 - 0 Fed 8 7

1

7 2

2

0 3.

a) CL Co3 -0 a) a ie 0 H,

1234 1234

20 days Fledged

Age of chick

Fig. 5. Effect on the weight of white-winged chough chicks (? SE, N) of food supplementation (O denote control groups; 0 denote experimental groups), age of the chick and hatch order. The lines depict the REML model estimates.

nest' competitive ability. Therefore, the weight hier-

archy within each brood was quantified by creating the variate 'relative weight' (dividing the weight of the chick by the mean weight of the nestlings in the

brood). A model of feeds to particular chicks was fitted

using the REML procedure. The square root of feeds

per hour was used as the response variable to nor- malize residuals. In the mixed model analysis initial

explanatory variables included: group as a random factor, experimental condition and laying date, which were treated as factors, and the continuous variates, group size, age of chick, and relative weight. All three-

way interaction terms, all terms including group size, all terms including laying date, and the interaction between relative weight and age of chick were discarded from the model (all P > 0-05).

As chicks approached fledging, groups fed young significantly more items per hour (change in deviance with 'day'; x2 = 10-3, d.f. = 4, P < 0.05). The number of feeds to each chick was dependent upon a significant interaction between experimental treatment and the relative weight of the chick (interaction term; X2 = 33-2, d.f. = 1, P < 0-001). Over the course of the

nesting attempt, control groups fed the heaviest chicks most, and lighter chicks received considerably less food. In contrast, the experimental groups fed lighter chicks more items than heavier chicks. Data are presented for 12-day-old chicks in Fig. 6.

Discussion

These observations and experimental manipulation cast light on three important problems in behavioural

ecology. First, they provide strong experimental support for previous descriptive evidence which suggested

0-4 0-6 0-8 1.0 1-2 1-4

Relative weight of chicks Fig. 6. The number of feeds per hour as a function of the relative weight of white-winged chough chicks when the oldest chick is 12 days old. In control broods (0), chicks larger than the brood mean (a relative weight greater than 1) receive more items than their smaller siblings. In contrast, experimental groups ()) feed the smaller chicks more items. Lines represent the REML model estimates for day 12, although those predictions have been back-transformed from the original model, which was calculated for square-root transformed data.

that white-winged choughs breed cooperatively because of foraging constraints. Second, they support the view that hatching asynchrony and food limitation are intimately linked to brood reduction in this species. Third, they suggest that brood reduction is sys- tematically manipulated by parents and helpers, rather than being a simple consequence of competition between unevenly matched siblings.

FOOD LIMITATION AND COOPERATIVE BREEDING

Cooperative breeding in white-winged choughs is not readily explained by the traditional models of habitat saturation or shortage of mates (Emlen 1991), because they are not territorial and their sex ratio does not deviate from parity (Rowley 1978; Heinsohn 1992). Instead, correlational studies have suggested that cooperative breeding in choughs is driven by diffi- culties in obtaining the food required to rear young, and in particular by the slow rate at which individuals acquire foraging skills (Heinsohn et al. 1988; Hein- sohn 1991a, 1992, 1995; Heinsohn & Cockburn 1994). Cullen et al. (1996) have also demonstrated that helpers continue to provide care to juveniles only if food is readily abundant. This evidence is strongly sup- ported by our food supplementation experiment: (i) in unsupplemented groups, relative contributions of group members increased with age, but when supplementary food was provided young birds tended to provision at a rate comparable to that of adults (Fig. 1); (ii) chough groups increased their nest pro-

50-, Order 1 2 3 4

10 days


15 -

10 -

5 9 Control 0 ~ 0 0O 0 0

0 A I I I

25 -

0

1

1

--



visioning rate (fourfold) in response to enhanced food

availability, over and above any effect of increased

group size (Fig. 2b). As previously reported by Heinsohn (1991a, 1992,

1995), chicks survived better as group size increased

(Fig. 3). However, the probability of nestling starvation was reduced even more dramatically by the

provisioning of food. Choughs rarely attempt to breed in pairs or trios, and inevitably fail if they do attempt to breed as a pair (Rowley 1978; Heinsohn 1991a). No pairs or trios hatched young in this study, but

predictions of the expected reproductive success of

pairs can be extrapolated from the linear relationship that exists between group size and fledgling output. Such extrapolation suggests that they would be suc- cessful if food was supplemented (Fig. 4). Therefore, Heinsohn's (1991a) hypothesis that choughs are obli-

ged to breed in cooperative systems as a result of their

foraging limitations receives strong support from this

experiment.

HATCHING ASYNCHRONY AND BROOD REDUCTION

White-winged choughs always show hatching asynchrony, and Heinsohn (1995) has argued that, consistent with Lack's original hypothesis, this provides the proximate basis for loss of young in broods provisioned by small groups. Although the brood reduction hypothesis has long been the preferred explanation for hatching asynchrony, in recent years it has been criticized (Forbes 1994; Stoleson & Beiss-

inger 1995; Stenning 1996). At least some of this criticism has arisen because of a lack of experimental testing of the hypothesis (Forbes 1994). While it is

necessary to manipulate hatching asynchrony in addition to food availability in order to test Lack's

hypothesis rigorously, our results in combination

strongly support the main tenets of the hypothesis. Foremost, groups of choughs breeding in poor food

conditions (control) reduced their broods more than

choughs in favourable (experimental) conditions. Almost 50% (20/43) of nestlings in control groups died. The primary reason for nestling mortality in

choughs is the inability to provide sufficient food. Control groups failed to allocate the necessary resources to late-hatched young; hence chicks in control groups always died in reverse order of their position in the brood hierarchy, so chicks that had accumulated the least parental investment died first. The only three chicks that starved in experimental groups were the lightest chicks in the brood. This was

probably because a small size hierarchy still existed within most broods. Therefore in all groups the first- hatched young benefited from significantly lower rates of mortality compared to their younger siblings (prediction 1).

A frequent criticism of Lack's hypothesis is that the

process of brood reduction is wasteful since parents

expend valuable energy on young which eventually starve to death (Clark & Wilson 1981, 1985; Amund- sen & Stockland 1988; Pijanowski 1992; Slagsvold, Amundsen & Dale 1995). However, the costs of brood reduction to chough groups are minimized provided the reduction occurs early. The pattern of chick mor-

tality over the course of the nesting attempt differed between experimental and control groups (Fig. 3). There were two distinct phases of nestling mortality recognizable in the control broods. The first phase, in which the period of greatest brood reduction

occurred, followed immediately after the last egg had hatched (day 4). Approximately 30% of nestlings in control groups died in this early phase. Sixty-five per- cent (13/20) of the nestlings that died did so before

they were 6-days-old. Feeding rates to chicks of this

age are extremely low (Fig. 2a). Choughs may produce a reasonably constant brood (three or four chicks), and then adjust the clutch size quickly (Heinsohn 1995). Very little parental investment is wasted if chicks die at this early age (prediction 2, Trivers 1974).

The second major phase of nestling mortality occurred between day 12 and day 22. Mean brood size decreased gradually throughout this interval, suggesting that the chicks died of starvation as group members could not deliver food items often enough. Thus, late brood reduction is costly as helpers invest considerable time and energy in young that starve to

death, and surviving chicks miss out on the additional

energy wasted on chicks that die.

Groups that quickly reduced brood size wasted less investment than those that attempted to feed too

many young. On average, surviving nestlings were

significantly heavier in broods in which reduction occurred prior to day 10 than in broods that were reduced later or not at all. With parental investment committed to fewer nestlings, those remaining obtained relatively more food and were better able to

grow and survive. In contrast, late brood reduction caused extended sibling competition, resulting in

underweight individuals at fledging, and a greater variation in body mass within the brood (Fig. 5). Con- trol groups that attempted to raise too many offspring jeopardized the condition of the young by causing lower body weights and therefore reduced their chances of surviving to independence (prediction 3). However, the weight hierarchy was almost eliminated at fledging in experimental broods (Fig. 5), either because of compensatory feeding by provisioning birds (Fig. 6), or because all young have grown sufficiently to attain an asymptotic weight at fledging.

In the experimental groups nestling mortality was

nearly eliminated (prediction 4). As a consequence, experimental groups did not suffer the drastic first-

phase brood reduction which characterized the control groups (Fig. 3; prediction 4). There is some evidence of a second phase of brood reduction. However, this apparent trend is partially an artefact of predation on two nestlings during this period. In all, very little





brood reduction is attributable to starvation in experimental groups.

Forbes (1993) suggested that brood reduction is

only an evolutionarily stable strategy when offspring fitness is higher following parental readjustment of effort. The results of this study strongly suggest that

hatching asynchrony is adaptive in choughs in that it facilitates early brood reduction in order to enhance the condition of the remaining offspring. Previous studies have found mixed results. As in this study, the

young from reduced broods benefited from significantly higher mean body mass compared to unre- duced broods in blue tits, Parus caeruleus L. (Slags- vold et al. 1995), and black-billed magpies, Pica pica (L.) (Husby 1986). In contrast, nestling pied flycatchers, Ficedula hypoleuca (Pallas), accrued no

weight benefits when the number of subordinate sib-

lings were reduced (Hillstrom & Olsson 1994). Chin-

strap penguins, Pygoscelis antarctica (Forster), and

great tits, Parus major L., that survived partial brood loss suffered a decrease in fledgling weight and recruit- ment rate (Moreno et al. 1994; Horak 1995). Thus while hatching asynchrony facilitates efficient brood reduction in choughs, in some other avian species it would appear that other factors may have been involved in the evolution of hatching asynchrony.

group intervenes to feed the lightest chick (Fig. 6; prediction 6), and as a consequence greatly diminishes the size hierarchy that ordinarily exists within the brood (Fig. 5). It is unlikely that this result is merely because the larger young were satiated. Nestlings were never seen to refuse food items, and invariably begged vigorously in response to an adult with food. By contrast, adults in experimental groups would appear to

bypass the attempts of the largest nestling to take food items from its bill in order to feed the smaller chick.

Further, there was evidence suggesting that some of the young chicks that died before day 6 in this study were the victims of active infanticide by adult group members (prediction 5). Most chicks died within five

days of hatching when their total food demands were

very low. Heinsohn (1995) found two nestlings, both less than a week old, alive on the ground below their nests. Both were the youngest in the brood. In addition, during this study a three-day-old chick still in the nest was found with multiple wounds on its

body and head. While siblicide does occur in many avian species (Mock 1984; Anderson & Ricklefs 1995; Osorno & Drummond 1995), it is unlikely that sibling rivalry was responsible for the injuries. The other nestlings were obviously too early in their development to have the means to inflict such injury upon their sibling.

DELIBERATE MANIPULATION OF THE FATE OF OFFSPRING


The standard model of brood reduction suggests that adults merely establish the brood hierarchy via hatch-

ing asynchrony, implying that the primary actors in brood reduction are the offspring (Lack 1968). However, it has been realized for some time that 'fierce

[sibling] competition will waste the energies of the brood... which spells a lowering of total surviving progeny. The behaviour of adult[s]... should tend to evolve so as to minimize this wastage' (Hamilton 1964). According to Hamilton, parents are the main actors in reducing brood size. More recently, there has been considerable debate on whether there is parent- offspring conflict over the final brood size, which could be dictated by the interests of adults, young, or both (O'Connor 1978). Nilsson (1995, p 255) reviewed the available experimental data on hatching asynchrony and concluded that most studies suggest that 'reduction of asynchronous broods is a consequence of the offspring being in a position to exert their will, which is possible due to the presence of one or more

easily outcompeted runts in such broods.' However, some studies report parental intervention in favour of the lightest, less competitive chicks (Parker, Mock &

Lamey 1989; Lamey & Mock 1991). The results of our experiment are suggestive of

manipulation by adults. In control broods, the lightest chick receives least food, as would be predicted by models of both adult and offspring control of brood reduction. However, in experimental broods, the

CONCLUSIONS

Food supplementation of white-winged chough groups tending nestlings profoundly improved chick

growth and survival, almost eliminating the attrition of nestlings that occurs in unsupplemented groups. Our results support previous correlational evidence for the skills hypothesis of cooperative breeding, and confirm previous evidence that failure to receive

adequate food is the principal cause of nestling mor-

tality (Heinsohn 1992). Our data support many of the

predictions of Lack's brood reduction hypothesis for

hatching asynchrony, and highlight the role of selec- tive allocation of food by parents in moderating chick survival under different conditions of food avail-

ability.

Acknowledgements

Nina Cullen assisted in crucial aspects of the field work. Sarah Legge, Rob Magrath, Penny Olsen, Anne Peters, Stephen Yezerinac, Tore Slagsvold and the Behavioural Ecology Group at ANU provided helpful comments on the manuscript.

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Received 18 October 1996, revision received 21 January 1997

? 1997 British

Ecological Society Journal of Animal

Ecology, 66, 683-691




Documents

Experimental Manipulation of Brood Reduction and Parental Care in Cooperatively Breeding White-Winged Choughs