Brood division in robins

Anim. Behav., 1985, 33, 466480

Brood division in robins D. G. C. H A R P E R *

Department of Zoology, Downing Street, Cambridge CB2 3EJ, U.K.

Abstract. Broods of fledgling robins Erithacus rubecula are sometimes divided between their parents so that each parent feeds only some of the chicks. These associations between a parent and certain of its young ('family units') are shown to be stable over periods of days. Brood division is most frequent in broods that are not followed by another nesting attempt. Experimental manipulation of the food supply suggests that brood division is relaxed when food is readily available. An analysis of the interactions between parents and chicks demonstrates that both adults and fledglings play a role in brood division. The possible functions of brood division are discussed with reference to 'other types of care', 'parental efficiency', 'cheat countermeasure' and 'two types of chick' hypotheses. Male parents feed chicks with shorter wingtengths than do females: since females tend to have shorter winglengths than males, this suggests that chicks are cared for by parents of the opposite sex. Possible causes and consequences of this observation are discussed.

In many species of birds both parents care for the young. There are reports in the literature that the broods of several species are divided between the parents after the young leave the nest so that each parent cares for only certain of its offspring. The species involved are taxonomically and ecologically diverse, ranging from great crested grebes, Podiceps eristatus (Simmons 1974) to ovenbirds, Seiurus aurocapillus (Hann 1937) and from whimbrels, Numenius phaeopus (Williamson 1946) to Darwin's finches, Geospiza spp. (Grant & Grant 1980). Such an association between a parent and some of its offspring has been called a 'family unit' by Nolan (1978). The functional significance of such a division of brood care between the parents is not clear (Simmons 1974; Nolan 1978; Smith 1978). Indeed the reality of the phenomenon is open to question. Most of the published reports of brood division are entirely anecdotal, although notable exceptions are the studies on prairie warblers, Dendroica discolor (Nolan 1978) and on song sparrows, Melospiza melodia (Smith & Merkt 1980). However the published data are not sufficient to provide convincing evidence that each parent cares for the same sub-set of chicks for periods of longer than a few hours (Hailman 1978). It is easy to envisage circumstances in which a parent might care for only certain of its young for short periods of time. For example, a parent might feed one particular chick until it was satiated and then transfer its attention to another individual. * Present address: Edward Grey Institute, Department of Zoology, South Parks Road, Oxford, OX1 3PS, U.K. 466

Such behaviour hardly warrants the application of the term family unit! In order to examine whether associations between a parent and certain of its offspring are stable through time we need to have observations of recognizable individuals that have been watched over long periods, rather than extrapolating from data collected over a few hours. Previous studies have experienced considerable problems in collecting the long-term data that are required. F o r instance, in dense vegetation it is often impossible to verify the identity of recently fledged young, even if they have been marked, which precludes making repeated observations on the same individuals (e.g. Smith & Merkt 1980). In suburban areas where birds are tame and the vegetation is often less dense than in natural habitats it is frequently possible to make very detailed observations on the behaviour of fledgling birds (e.g. Snow 1958). In this paper I report some observations on the parental care of fledglings in a suburban population of robins (Erithacus rubecula) hiving in a suburban environment. Evidence is presented for brood division that is stable over most of the fledgling period and the rote of the adults and chicks in maintaining this division is assessed. Finally I discuss some possible functions of this behaviour.

METHODS

These observations were made during 1981 and 1982 in the Cambridge University Botanic Garden.

Harper: Brood division in robins All individuals were marked with unique colour ring combinations: the young included in the data were all ringed as nestlings about 6 days after hatching. The birds were all well habituated to my presence and detailed observations were further facilitated by the generally sparse ground cover. Records were collected using a stopwatch, notebook and tape-recorder.

Fledging Behaviour The age at which chicks left the nest, to the nearest day, was determined for 163 individuals in 39 broods by monitoring nests on a daily basis. The day on which a chick ftedged was called day 0 for that individual. It has been suggested that in song sparrows the parents sometimes begin to divide the feeding of the brood between themselves as soon as the chicks begin to fledge (Smith & Merkt 1980). Therefore I observed the departure of at least part of six broods from the nest and recorded how many feeds each parent took to the nest and to each individual fledgling during the actual course of fledging. It was not possible to see which individuals received the food taken to the nest.

Feeding of Fledglings Ten broods were studied in detail. These broods initially contained 40 fledged young and 22 of these reached independence. Fledgling robins are dependent upon their parents for between 17 and 23 days after leaving the nest (Lack 1943; East 1981, personal observation). Initially they are virtually immobile, but they become more active about 6 days after fledging. To facilitate comparisons between chicks at different stages of development I have divided the dependent period into three sections: day 0 to day 5, day 6 to day 11 and day 12 onwards (all inclusive). Five of these broods were followed by other breeding attempts by the parents in the same year and I shall refer to these as 'Early' broods. The other five were the final attempts made by the pair that season and I shall refer to these as 'Last' broods. Each brood is identified by a capital letter (e.g. A, B) and each chick within a brood by a number (e.g. D3). Broods H and K were successive attempts by the same pair. Each chick in these broods was observed for 60 rain on alternate days fi'om the day on which it fledged until it either died or became independent

467

of its parents. All observations were made between 0600 and 1800 hours GMT and chicks were allocated to observation periods on a systematically random schedule. Not all of these 60-min samples were continuous records since I occasionally lost contact with the focal chick or failed to see the parent's colour rings (N= 6). However no sample took longer than 75 min to collect and no breaks in observation exceeded 5 min. Therefore the biases caused by certain behaviours tending to occur out of my sight should not be large. During observation periods I noted every occasion on which the chick came within I m of either of its'parents. The following details were recorded. (a) The identities of th e parent and chick. (b) The age of the chick in days after fledging. (c) Which individual made the approach (defined as the movement that brought parent and chick within 1 m of each other). (d) Which individual caused the separation (the movement increasing the distance between parent and chick to over 1 m). (e) Was the adult carrying food? On several occasions I overlooked food in a parent's bill which was revealed when fed to a chick. The data therefore underestimate the frequency with which adults were carrying food. (f) Did the chick beg? (g) Did the adult feed the chick? (h) Did the adult attack the chick? In order to test the hypothesis of brood division I have used the rates at which parents fed their chicks as a crude measure of parental care. If a brood is divided between its parents so that each adult tends to feed only certain of its offspring we can make two simple predictions. Firstly each individual chick will (usually) receive unequal numbers of feeds from its two parents. This would also be the case if one parent makes a smaller contribution to feeding the whole brood and distributes this limited food at random. The second prediction is that the proportion of food an individual chick in a divided brood receives from a particular parent will not be the same as the proportion of feeds to the whole brood made by that parent. Note that it would be possible for only the second of these predictions to hold. This would happen if one parent fed only a limited number of chicks but shared the feeding of these chicks equally with its mate. Such cases of brood division in which all the chicks are receiving a substantial amount of food from the same parent

468

Animal Behaviour, 33, 2

are clearly not as extreme as cases in which there are some chicks receiving most of their food from their father and others receiving most from their mother. I have therefore used the data on feeding frequency to test two null hypotheses for each chick: Hypothesis A: The chick was fed equally by both parents. As noted above the rejection of this hypothesis is not evidence for brood division. Under this null hypothesis the probability that X out of N feeds were made by the male is given by the following binomial expression: x N! P (X/N) = i=0 ~ i! ( X - i)~"0.5u

the chick is a member of a family unit. I shall refer to a chick and that parent which feeds it most frequently as an 'in-chick' and its 'in-parent'. A chick which is fed by a particular parent less often than the average brood member is referred to as being one of that parent's 'out-chicks'. Details of interactions between chicks and their parents in undivided broods will be given elsewhere. Statistics follow Siegel (1956): Mann-Whitney U-tests and Kruskal-Wallis tests have not been tie-corrected and are thus conservative.

RESULTS (For details about the binomial distribution see Sokal & Rohlf 1969.) Hypothesis B: The proportion of food the chick received from the male was equal to the proportion of food the whole brood received from the male. If this hypothesis is rejected there is evidence for brood division and hypothesis A can be used to test whether or not a particular chick receives most of its food from one parent. Under this hypothesis the probability that X out of N feeds were made by the male is given by the following binomial expression: x N! P (X/N) = i=0 ~ i! (N-i)! "qN'(1 _q)N-x where q is the proportion of feeds to the whole brood made by the male. Additional data are available for 19 other broods watched in considerably tess detail. These broods were watched casually and for each brood I have pooled all the feeds made by a parent to a chick. If the proportion of feeds delivered by the male was such that it was possible to reject hypothesis B at the 0'05 level for a least two brood members, I decided that there was evidence for brood division. The observation that an individual chick is fed more often by one parent than by the other could arise in any combination of three ways. (a) The chick encounters its parents at different rates. (b) The chick is more likely to beg for food off one parent when it encounters it than it is to beg off the other parent. (c) One parent is more likely than the other to feed the chick when it begs for food. In order to determine which of these factors are associated with brood division in robins I analysed the data on parent-chick interactions for all the cases in Table III for which there is evidence that

Fledging Behaviour The median age at fledging was 13 days (99% confidence limits 12 to 14, range 10-15). In only two broods did I find any evidence that some chicks (N = 3) left the nest on the day before their siblings, and all broods fledged within a period of 18 h (unless some chicks left during the hours of darkness which seems unlikely). Table I summarizes the observations made upon the six broods observed during the course of fledging. In one brood there is evidence that the two members of a pair differed in the rate at which they fed the brood (brood B, binomial test P<0.05). However in most broods females seem to feed the young that are still in the nest at a higher rate than do males (pooled data, binomial test, P<0-001; data for broods B, C, E and F each significant at the 0.05 level). Five individual fledglings (B1, B3, C1, F 1, F2) were fed significantly more often by their father than by their mother (binomial test, P~<0.05).

Feeding of Fledglings in the Broods Studied in Detail The rate at which a chick receives food from its parents decreases as it grows older (Fig. 1). This decline in parental feeding is associated with an increased rate of self-feeding by the chick (personal observation) and has been reported previously by East (1981). Note that Early broods tend to be fed at a higher rate at a young age than do Last broods. This might reflect a decrease in food availability late in the season. Table II gives the proportions of feeds made by the male to the fledged brood during three stages of the dependent period. When making comparisons

Harper: Brood division in robins

469

Table I. Allocation of feeds given to young during the course of fledging by male and female robins Number of feeds to young Outside nest Observation In nest period (min) M F Brood A B C D E F

24 240 180 93 180 210

1 M

2

F

10 02 3 17"** 21 0"** 11 21"* 7 0"* 78 11 9 17" 3 4 6 19"* 11 4*

M

F

10 9 7 5 1 01 3 1 7 0"*

3 M

4 F M

5 F M

F

00 5 0

-1 0

-0 0

01 2 0 4 4

-1 1 --

--

M, F: no. of feeds delivered by male and female respectively. Young are numbered in the order of leaving the nest. Since the nest contents were not visible, all feeds to the nest by each parent have been pooled. * P<0.05, **P<0.01, ***P<0.001; binomial test between male and female feeding rates.

it is important to exclude the value for pair M in the final period, since the female of this pair had by this stage deserted her mate. The table reveals that males make a significantly higher contribution to feeding young in Early broods than they do to those in Last broods. Moreover the proportion of feeds which are made by the male increases with time for Early broods (Kruskal-Wallis test, H = 6 - 6 1 5 , df=2, P < 0 - 0 5 ) but does not do so for Last broods (Kruskal-Wallis test, H = 0 . 3 1 8 , df=2, P> 0.10). This is presumably because all the females with Early broods had laid a new clutch and begun incubation before the fledglings became independent. In fact it is surprising that these females fed the young as often as they did; both Lack (1943) and East (1981) have stated that fledglings from such broods are fed almost exclusively by the male, although neither gives any details. If this difference between populations is genuine, it may reflect differences in habitat since both Lack (1943) and East (1981) studied rural populations. It is possible that in rural areas males are able to rear fledglings alone more easily than they can in gardens, perhaps as a consequence of differences in food availability. Females beg for food off their mates from shortly before clutch initiation until the end of incubation (Lack 1943; East 1981; personal observation). At first sight it seems energetically inefficient for the female to both beg for food offher mate and to help him feed chicks. On seven

occasions I observed a hen giving food she had received from her mate to a fledgling. Such apparent inefficiency strongly implies that the transfer of food from male to female represents more than a transfer of kilojoules: for example, it may be important for pair-bond maintenance (Harper 1984). Table III shows the proportion of feeds made to each individual chick by its father during the three stages o f the dependent period. Since males make a greater contribution than females to the feeding of Early broods, it is not surprising that 15 of the 16 chicks from Early broods that were fed more often by one of their parents were fed most often by their father. The exception, G3, was a member of the only Early brood for which there is evidence of brood division and continued to be primarily dependent on its mother even after she started incubation. Four of the five Last broods in Table III were divided (hypotheses A and B rejected); six of the chicks involved were fed preferentially by their mother and five by their father. Note that brood E shows no sign of brood division at all. Family units are clearly stable for long periods: each cell in Table III is the result of pooling at least 180 min of observation that were spread over a period of at least 5 days. Note that only one of the 22 chicks reaching independence was not seen being fed by both parents. This exception (L4) was

Animal Behaviour, 33, 2

470

141

Table II. Proportion of feeds made by male in different broods at different chick ages

12

- -

Early

....

Last

Chick age (days after leaving nest) Brood

10-

1

8"

6'

4-

9 2"

0

,

,

0

2

i

,

i

i

4

6

8

10

6-10

12 +

Early broods G 0.59 (139) Ct 0.59 (130) H:~ 0.8 (108) Dt 0.50 (111) I 0-65 (57)

0-63 (87) 0.84 (76) 0.97 (65) 0.73 (71) 1.00 (30)

0.65 (49) 0.88 (32) 1.00 (29) 0.94 (36) 1.00 (19)

Last broods J K:~ L Et M

0.67 (57) 0-42 (73) 0.60 (53) 0.51 (59) 0.49 (65)

0.59 (29) 0.48 (29) 0.59 (23) 0.54 (28) 1.00 (41)*

1 P<0.01

0 P<0.01

0-49 (98) 0.54 (111) 0.59 (81) 0.53 (116) 0-48 (79)

Mann-Whitney test U 4 P P<0.05 12

14

16

18 20

22

Chick age (days after fledging) Sample sizes :

Early

20

16

13

12

12

12

12

12

11

11

9

7

Last

20

18

18

16

15

14

13

12

11

9

5

0

NS

~

~

~:~

NS

NS

NS

NS

NS

NS

~

0-4

Figure 1. Rate at which chick fed by parents plotted against chick age for Early and Last broods. Values plotted as medians with total ranges represented by vertical lines. Sample sizes and the significance levels for Mann-Whitney U-tests between Early and Last broods are given below the horizontal axis (ys:P>0.05, *P< 0.05, **P< 0.01).

an unusual case since it was born on a neighbouring territory and was adopted by the male on the day it fledge& Most fledglings are fed by both parents in that few broods seem to be divided until several days after fledging (only brood J provides a clear example of early division, although there are signs in brood G). Thirteen of the 22 chicks reaching independence had been fed exclusively by one parent in at least one sample period. Although brood division is relatively stable over periods of days, family units are not immutable. For example, I did not see the mother of chicks J3 and J4 feed either of them until after both the chicks she had been feeding were dead. The male of brood M was deserted by his mate 11 days after their young had fledged and promptly began to feed chick M1 which I had not seen him do for 7 days. Brood M demonstrates that brood division need

* Female of pair deserted on day 11. t Brood also in Table 1. Successive attempts by same pair. Sample sizes are given in parentheses. not involve all the brood members: chick M2 was fed frequently by both adults while its two siblings were being fed by only one parent.

Feeding of Fledglings in Other Broods Additional data are available for 11 Early broods and eight Last broods. These suggest that Early broods are divided less frequently than Last broods (hypothesis B rejected for one Early and five Last broods, Fisher exact test, P < 0"01). Note that since the data were pooled over the whole dependent period these figures will underestimate the frequency of brood division. There is no tendency for parents of one sex to feed a greater number &chicks (pooling data from Table III and the additional broods, 18 chicks fed mainly by males and 15 by females, binomial test, P>0-10).

Parent-offspring Interactions in Divided Broods Figure 2 shows the median encounter rates (together with observed ranges) for parent/in-chick and parent/out-chick dyads at the three stages" of the fledgling period. Chicks were always encountered most frequently by their in-parent (days 0 to

Harper: Brood division in robins

471

Table III. Allocation of feeds by parents during fledging period: proportion of feeds made by male Early broods

Last broods

Chick age (days post-fledging) Chick G1 G2 G3 G4 G5 C1 C2 C3 H1 H2 H3 H4 D1 D2 D3 D4 I1 I2 13 14

0-4 26/36** 29/38i* 4/35-~T 7/9 16/21" 16/37 19/35 26/31~77 13/16" 24/28*** 27/33*** 27/31"** 12/33 15/29 18/29 11/20 5/8 3/9 7/8* 22/32*

6-10 27/27~ 28/28T~~ 0/32777 --24/32* 19/21"** 21/23"** -29/29*** 28/29*** 6/7 18/22"* 17/27 17/22" ----30/30***

12+ 17/17T~~ 13/13~* 2/19~ --11/12"* 10/13" 7/7** -16/16"** 13/13"**

Chick age (days post-ftedging) Chick

Jl J2 J3 J4 K1 K2 K3 K4 L1 L2 L3 L4w 8/8** El 12/14"* E2 14/14"** E3 E4 -E5 M1 -M2 19/19"** M3

0-4

6-10

12+

1/24~T~ 0/227~~ 22/27~i~ 25/25-~T 19/33 12/27 15/26 14/25 8/11 12/27 12/27 16/16TT 7 5/9 14/30 15/26 12/27 16/24 15/25 11/27 12/27

-2/217"* 19/19~ 17/17~i~ 1/23~ 1/19TT~ 5/7 24/247~7 -3/16" 0/18~ii 19/197t~ -I0/20 -13/20 7/19 0/21777 11/23 21/217~ ~

--7/17 I0/12" 0/3 1/137~ 13/13~* --1/127" 1l/117~* -5/10 -7/10 3/8 16/165 13/13' 12/125

Significance levels at which hypothesis A can be rejected: *P<0.05, **P<0.01, ***P<0.001. Significance levels at which hypothesis B can be rejected: ~P<0.05, tiP<0'01, t]~P< 0'001. $ The female of this pair deserted on day 11. wThe chick was born on a neighbouring territory and adopted by the male of pair L. 4, N = 8, N ' = n u m b e r of chicks encountering inparent most o f t e n = 8 , binomial test, P < 0 . 0 0 1 ; days 6 to 10, N=N'= 13, binomial test, P < 0.001; days 12+, N = N ' = 7 , binomial test, P<0.001). The rate of encounter between parents and their in-chicks declines during the fledgling period (Kruskal-Wallis test, H = 19.035, df= 2, P<0.001), but shows no significant change for parents and their out-chicks (Kruskal-Wallis test, H = 5.338, df=2, 0.10> P > 0.05). Figure 3 shows the percentage of approaches that were made by the chick ( ~ A p ) , the percentage of separations that were made by the chick (KS) and the difference between these two percentages ( ~ A p - ~S) plotted against chick age for in-chicks and out-chicks. There is no evidence that the role played by the chick in making approaches differs between in-chicks and out-chicks during any time period (Mann-Whitney U-test, P > 0-10). The only significant difference between the roles of in-chicks a n d out-chicks in initiating separations was that

following the 12th day from fledging in-chicks were more likely to be responsible for a separation than out-chicks (Mann Whitney U-test, see Fig. 3). The proportions of both approaches and separations caused by the chick increased during the fledgling period (Kruskal-Wallis tests: ~oAp, H = 10.863, df=2, P < 0.01; ~oS, H = 12.117, df=2, P<0.01). This is hardly surprising since recently fledged chicks are virtually immobile. Indices of the form ~ A p - - ~ S have been used in several studies as a measure of the role of two social partners in maintaining proximity (see Hinde & Atkinson 1970). The value of this index changed with time in the present study (Kruskal Wallis test, H = 7.699, df= 2, P < 0"05) suggesting that the chick's role in maintaining the limited proximity between itself and its parent was greatest during the middle of the fledgling period. Note that the value of the index must approximate to zero when one of the partners is largely immobile, as is the case for recentlyfledged robins. It is therefore impossible to inter-

Animal Behaviour, 33, 2

472

10

8

t-

6' r 0

or

4

UJ

0 0-4

6-10

12+

Chick age (days affer fledging) Sample sizes :

8

15

7

Figure 2. Rate at which chicks encounter their parents (at distances of less than 1 m) at different ages for parent/inchick and parent/out-chick dyads. Data plotted as medians together with total ranges represented by vertical Iines. Sample sizes are given below horizontal axis. pret indices of this type without reference to the absolute values of %Ap and %S (as the figure in Hinde 1977 accidentally demonstrates). Moreover this type of index ignores the possibility that the partners are responding to subtle cues from each other (for a discussion of these problems see Hinde 1979). Adults that encountered chicks at distances of less than 1 m were usually carrying food. Table IV includes data on the probability that an adult was carrying food when it encountered a chick. Throughout the fledgling period parents were more likely to be carrying food when they encountered an in-chick than when they encountered an outchick (days 0 to 4, Fisher exact test, P < 0-001; days 6 to 10, Z2=85.597, df= 1, P<0-001; days 12+, Z2= 19.235, df= I, P<0.001). The probability that a parent was carrying food when it encountered an

in-chick decreased as the chick became older (Z2= 48.405, df= 2, P < 0.001), but this was not so for encounters with out-chicks (Z2=3.594, df=2, P>0.10). Table IV includes data on the probability that a chick begged at a parent during an encounter. Recently-fledged chicks (days 0 to 4) nearly always begged at either of their parents, whether or not the parent was carrying food. However older chicks were more discriminating. Firstly they were more likely to beg if the parent was carrying food than if it was not (Fisher exact tests: days 6 to 10, in-chicks, P<0.001, out-chicks, P<0.001; days 12+, in-chicks, P<0.05, out-chicks, P<0.01). Secondly older chicks were more likely to beg at their in-parent that at their out-parent (comparing the responses of in-chicks and out-chicks to adults with food: days 6 to 10, Fisher exact test, P < 0-001; days 12 + , Fisher exact test, P < 0-001). Inspection of the data suggests that these results are not caused by one or two chicks in the sample: only one cell in Table IV (where N = 3) includes records from fewer than seven individual chicks. It seems that chicks may become more adept as they get older at predicting whether or not a parent will feed them and stop begging if they judge that they are unlikely to be fed. Table IV also shows that chicks became less likely to beg as they grew older (Fisher exact tests comparing chicks of under and over 11 days of age, cases in which adult carrying food: in-chicks, P < 0"001; out-chicks, P < 0-001). Table IV also includes the probability that an adult that was carrying food fed a chick that was begging at it (I never saw a parent feed a chick that was not begging). Parents nearly always fed their in-chicks in these circumstances and the probability that they did so remained roughly constant as the chicks grew older (Fisher exact test, P > 0" i0 between time periods). At all chick ages parents were much less likely to feed out-chicks than in-chicks (Fisher exact test, P < 0.001, for all three time periods) and the probability that they did so decreased with time (comparing days 0 to 4 with the later observations: Z2= 23"343, df= 1, P < 0.001). Parents very rarely strike their own young: only 10 of the 710 encounters between parents and their in-chicks involved aggression, while parents were only seen to strike out-chicks during two out of 170 encounters. These proportions are not significantly different (Fisher exact test, P > 0-10). Brood division does not seem to be maintained by the parents behaving aggressively towards out-chicks.

Harper: Brood division in robins (n) % Ap

% 1001

9 In-chick % 100o Out-chick

tt

50-

0-~

(b) %S

(NI=Nz)

8

(c) % Ap- % S

50

6210 12'-t13

% 100'

50

6-'10 12'+ age (days offer fledging) 0-4

Chick Sample sizes

473

7

8

Mann-Whitney U 32 77.5 17,5 P>0.10 P > O A O P > 0 . 1 0

13

0'-4 6-10 12"+

7

6

50 "/'2.5 10 P > O . I O P > 0 . 1 0 P
13

7

26.5 58.5 18,5 P > O . I O P > O . I O P > O , IO

Figure 3. Comparison of individuals' roles in making approaches and leavings in parent/in-chick and parent/out-chick dyads at different ages. (a) Percentage of approaches made by chick (%Ap). (b) Percentage of separations made by chick (%S). (c) Difference between these two percentages (%Ap-%S). In all cases the data are plotted as medians together with total ranges represented by vertical lines; sample sizes and the results of Mann-Whitney tests comparing the two dyad types are given below the horizontal axis. Table IV. Summary of interactions between parents and chicks

DISCUSSION

Occurrence of Brood Division Chick age (days out of nest) Dyad type 0-4

Parent had food?

Chick begged?

Chick fed?

In-chick

Yes 201 Yes 201 Yes No 3 Yes 3 Out-chick Yes 28 Yes 26 Yes No 12 Yes I1 In-chick

199 19

6-10

Yes 311 Yes No 18 Yes Out-chick Yes 48 Yes No 38 Yes

309 Yes 285 ll 39 Yes 5 6

12+

In-chick

139 Yes 15 7 Yes 2

Yes No Out-chick Yes No

145 32 22 22

Yes Yes Yes Yes

137 4

Data are divided according to whether or not the chick was that parent's in-chick, whether or not the parent was carrying food, whether or not the chick begged and whether or not it was fed. Note that it is logically impossible for a chick to be fed by a parent that is not carrying food and that it was empirically determined that chicks always begged when fed. The Table is therefore truncated since all missing values can be obtained by subtraction.

Robin broods are sometimes divided into family units: certain fledglings tend to be fed by one parent. There is no evidence that a similar division of labour occurs in the other forms of parental care given to fledglings; in particular both parents will mob potential predators approaching any of their brood (Harper 1984). The ways in which parents allocate feeds to individual fledglings in three species o f passerines are described in Table V. The robins in this study differ from the prairie warblers and song sparrows in several ways. In the other two species brood division seems to be more marked immediately after fledging than it is in robins. Smith & Merkt (1980) point out that the simplest mechanism leading to brood division is that family units form as the young separate at fledging. Despite the fact that parent robins often differ in their allocation of feeds to the members of their brood (Table I), this does not always result in brood division. F o r example, chick C 1 was fed significantly more often by its father while its siblings were still in the nest. However for the first few days of its fledgling life it

474

Animal Behaviour, 33, 2

Table V. Formation and sta_bilityof family units in three passerine species

Prairie warbler (Nolan 1978) Proportion of broods leaving nest on same day

~<96%

Allocation over first few Family units form days when chicks relatively "within a few hours' immobile

Song sparrow (Smith 1978; Smith & Merkt 1980)

Robin (this study)

~<53% At least 47% leave over 2-day period

~<95% 100% leave within 18 h of each other

Some family units formed immediately; about 80% of young fed by one parent

Brood division not as extreme early on; about 10% of young fed by one parent

Allocation as chicks become mobile

Family units 'stable'; Males take over Brood division occurs in unless female re-nests responsibility for some broods. Most common all fed by male some young even if in broods not followed by mates do not re-nest. re-nesting. Male's role More sharing of young in feeding increases if female by parents. Females re-nests. Females continue may continue to feed to feed one young while one young while incubating incubating

Proven stability of family units

No quantitative information

was fed about equally by its two parents, its father devoting a disproportionate n u m b e r of its feeds to the last chick to leave the nest, C3 (Table III). The proportion of feeds given to fledgling song sparr o w s that are from their father increases as the chicks grow older, regardless of whether or not the female re-nests. This contrasts with the robins in which the male's contribution only increases if his mate makes another breeding attempt. Snow (1958) considered brood division to be potentially disadvantageous because if one parent was lost then the other might be unwilling to take over the whole brood. However in both song sparrows (Smith 1978) and robins the loss of one parent has been followed by the survivor feeding young it had previously ignored (e.g. the deserted male of brood M). One reason for this willingness to feed any chick when the need arises may be that very few, if any, juveniles reach independence without being fed as fledglings by both parents. 'Perfect' brood division may be selected against since it has risks, as envisaged by Snow (1958).

Parent-chick Relationships in Divided Broods Chicks in divided broods have very different

At least 120 rain, probably longer

Several days

relationships with their two parents: (a) they encounter their in-parent more frequently; (b) their in-parent is more likely to be carrying food when encountered; (c) they are more likely to beg for food offtheir in-parent; and (d) they are more likely to be fed when they beg off their in-parent. The higher encounter rate between parents and their in-chicks could arise in two different ways. Firstly individuals may be able to recognize each other at distances of greater than 1 m and may only tend to approach members of their own family unit. Secondly the two family units may tend to use different areas of the territory, so that an individual would be more likely to encounter members of its own family unit even if its movement was random. Obviously these two hypotheses are not exclusive. I have no evidence that parents and their in-chicks move around together. Indeed all members of the family tend to avoid each other, possibly to reduce interference during foraging (Harper 1984). If the two family units were spatially separated, chicks should meet their in-parent's other in-chicks more frequently than the other brood members. This prediction can be tested for 12 cells in Table III involving eight individuals (days 0 to 4: J1, J2, J3, J4; days 6 to 10: G I , G2, J3, J4, K1, K2; days 12+: G1, G2). I have extracted from the detailed beha-

Harper: Brood division in robins vioural records the rates at which these individuals encountered their siblings at distances of less than 1 m. The median rate at which these chicks encountered members of the same family unit was 2.2 per sibling per h (range 0-5-7), while that for members of the other family unit was 2.5 per sibling per h (range 0-5.2). There were 10 cases in which the chick encountered members of the two family units at different rates (Jl and J2 were not seen to encounter siblings): in six of these cases the chick met its in-parent's out-chicks more often than it met members of its own family unit (binomial test P>0-10). This provides some support ~br the hypothesis that parents encounter their in-chicks more often than their out-chicks as a result of at least one member of the dyad recognizing the other and tending to approach it. F o r the first few days of fledgling life the chicks do not play a very important role in influencing brood division. Their immobility means that it is the parent who determines the rate at which it encounters a particular chick, and there is no evidence that young chicks can discriminate between their parents. However parents seem to be able to discriminate between their young at this early age since they are significantly less likely to feed out-chicks that beg at them than in-chicks. One potential cue that the parents could use to discriminate between young fledglings is their location in the territory which tends to be highly predictable (Harper 1984). Once the chicks have become more mobile, both they and their parents play a role in the rate at which particular parent/chick dyads encounter each other. Since the chicks are no longer predictably located the parents must be using different discriminatory cues. Although individual recognition is a possibility, they may be simply categorizing the brood. For example the male might feed the small chicks and the female large chicks. A series of experiments on individual recognition in robins will be reported elsewhere. The fact that the chicks are more likely to beg for food from their in-parent than their out-parent raises the possibility that they are capable of recognizing their parents as individuals. Alternatively they may be responding to subtle differences in their parents' behaviour, not bothering to beg if they can detect that they are unlikely to be fed. Functions of Brood Division

The species suggested to practise brood division

475

seem to share little in common (see Introduction). Some have precocial young, others altricial; some feed their young, others do not. As pointed out by Smith (1978) the phenomenon of double-clutching (in which a female lays two clutches, each of which is incubated by one member of the pair who tend separate broods, e.g. Portal 1924) can be considered to be an extreme example of brood division. Faced with such a diversity of behaviour it would be rash to seek a single function for brood division. The fact that only some broods of robins are divided suggests that brood division has both benefits and costs, and that in some circumstances it is to the advantage of the parents and/or chicks, while in others it is not. There are four possible advantages that could be associated with brood division which I wish tO discuss. These potential benefits need not be exclusive, nor are they all equally applicable to all instances of brood division.

(1) "Other types of care' hypothesis Reports of brood division in species that do not feed their young (e.g. Williamson 1946) emphasizes that, although I have detected brood division in robins by observing the parents feeding their young, the function(s) of this behaviour may be totally unrelated to parental feeding. Species that do not feed their offspring frequently lead them to feeding sites. If brood division in these species was accompanied by the physical separation of the two family units, it could reduce competition between brood members for food. In addition brood division might reduce the risk that the whole brood is predated. The hypothesis that brood division facilitates the provision of a pattern of brood care other than parental feeding is difficult to accept in the specific instance o f the robin since the members of the brood seem to mingle freely with one another.

(2) "Parental efficiency' hypothesis The idea that brood division is an adaptation that promotes parental efficiency has been a popular one. However, exactly what is meant by parental efficiency and the precise mechanism by which parental efficiency is increased by brood division has never been clearly explained. It is clear that many authors equate increasing parental efficiency with increasing the rate at which the chicks are fed. However anecdotes about parents spending considerable time and energy searching for an in-chick while ignoring nearby out-chicks begging for food

476

Animal Behaviour, 33, 2

(Snow 1958) suggest that the very reverse is the case. Smith (1978) considered that 'it is clearly easier to locate two young rather than four'. This can only be true if chicks tend either to be predictable in location or to follow their in-parent about. If a parent cannot predict where it can find its in-chicks, then it will clearly be more difficult to find one of two specific young than any member of a brood of four. Fledgling robins are highly predictable in location when recently fledge& When they are more mobile it is probable that the parents use the chicks' begging calls as a cue to their location. Brood division in robins seems to become more marked as the young become older and more mobile. In other words, most cases of brood division in robins seem to occur when the potential costs to the parent of searching for an in-chick are highest. Simmons (1974) stated that brood division in great crested grebes results in a higher rate of feeding of individual chicks. Unfortunately no data were published. Attempts to analyse the robin data to determine whether chicks in divided broods are fed at a faster rate are complicated by the steep decline in the rate of feeding with chick age and by the evidence for seasonal variation early on in the dependent period (Fig. 1). However there is no trend for chicks in divided broods to be fed more than those in undivided broods (see Table III). Obviously the sample sizes are small and more data are required to test this hypothesis adequately. The expectation that feeding rates will be higher in divided broods is a little naive. Assuming that brood division increases parental feeding rate and that it also has costs, it is possible that it will only occur in those pairs that could not otherwise achieve a high enough feeding rate. The net result of this feeding-rate-dependent brood division could be that there was little variation between pairs in parental feeding rate. There is some evidence that brood division in robins is related to parental feeding of chicks. For reasons to be discussed elsewhere, I gave some pairs of robins an ad libitum food source (bowl of maggots) for a period of 4 h while they were feeding fledglings. The feeds made by each adult were recorded for 20 min (each adult separately) every hour for 8 h (two before, four during and two after the exposure to extra food). I had evidence that two of these broods, G (tested on day 7) and J (day 9), were divided. Figure 4 shows the unexpected result

before

after

during

G1

i

o

I

1

I

J1 .A

-2

-1

0

1

key

2 hours

3

4

I

I

5

6

I--~female lmale

Figure 4. Allocation of parental feedings before, during and after the experimental provision of food to pairs of robins feedingfledged young. No observations were made during the third hour after the food was added. of this extra supply of food: a temporary relaxation of brood division. While the food was made available none of the seven chicks was fed exclusively by one parent. The proportion of feeds received from their mother is significantly related to the provision of extra food for all of the chicks (Fisher exact tests, P ~<0.001 for all except J2 where P < 0-05). When the food supply was removed the parents reverted to the same in-chick as before; a further indication of the underlying stability of family units. The hypothesis that food abundance influences the occurrence of brood division has been previously advanced by Simmons (1974) who suggested that great crested grebes divide their broods sooner after fledging if food availability is low. This observed relationship between food availability and brood division in robins may partly explain why the frequency of brood division is more frequent late in the season (when food availability may be low) and why it has not been detected in other habitats (Lack 1943; East 1981). Although the relaxation of brood division when

Harper: Brood division in robins food is readily available is consistent with the parental efficiency hypothesis, it is also consistent with other hypotheses (see below). If the feeding rate hypothesis is correct, there must be some unidentified cost of brood division preventing it occurring in all robin broods.

(3) 'Cheat countermeasure' hypothes• If both parents feed their whole brood at random the potential variation in food intake between individual chicks will be considerably greater than if each parent feeds part of the brood at random. Consider two parents who each allocate 10 feeds randomly to a brood of four. If the brood is not divided the number of feeds any one chick could receive ranges from 0 to 20. However, if the brood is divided the maximum number of feeds an individual can receive is only 10. Figure 5 illustrates how the chicks in the divided brood are less likely to receive a small number of feeds. Thus brood division leads to a more equal sharing of food resources between siblings and reduces the probability that any starve to death. Although this is clearly in the parents' interests it need not necessarily be in the chicks' interests. Individual chicks should benefit from 'tricking' their parents into giving them more than their fair share of available food. If both parents feed a particular chick neither of them will be able to make a reliable estimate of its total food intake. However if only one of them feeds each chick they will be in a better position to assess the chick's food intake and potentially less

0.25

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0.20

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.

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.

.

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.

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.

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.

.

likely to be manipulated into giving that chick too much food to the detriment of its siblings (and therefore the parent). It is unknown whether or not adult robins are capable of making this kind of assessment. However the important point is that brood division could, in theory at least, be a parental strategy to minimize the costs the chicks can inflict by 'cheating'. When the recently-fledged young are relatively immobile it might be easier for their parents to monitor the food intake of individuals and to minimize cheating by the chicks. For instance by taking food to the chicks' locations in sequence they could reduce the variations between individual chicks' food intake. As the chicks become more mobile this strategy would become decreasingly effective. If brood division functions in a similar manner it would be predicted to become more marked as the chicks become mobile. The data in Table III suggest that this is so; in the first 4 days of fledgling life hypothesis B can only be rejected for seven out of 40 chicks, but between days 6 and 10 it is rejected for 13 out of 29 chicks (Z2= 6' 115, df= 1, P < 0-05). Inequalities in feeding rate between siblings will be most marked in data sets collected over short time periods since the same individuals are unlikely to be fed consistently more often than their siblings whether by chance or as a result of cheating. To test adequately the hypothesis that brood division reduces the variation in feed rate between siblings, much more detailed data are required than are currently available. The present evidence suggests that any reduction cannot be large. Table VI summarizes the results of a nested one-way analysis of variance that compared the variance in feed rate within broods with that between brood. Data were used from Table III for all eight broods that contained three chicks 6 days after leaving the nest Table VI. Nested one-wayanalysisof variance of the rates at which individual chicks were fed on day 6

--~

0 1 2 5 4 5 6 7 8 9 10

477

:

-

/>11

Numberof feeds

Figure 5. The probability that a chick in a brood of four receives a certain number of feeds when (a) both parents feed the whole brood at random with 10 feeds (not divided) and (b) each parent feeds a family unit of two chicks at random with 10 feeds (divided). See text for explanation.

Source of variation

df

Sum of Mean squares square

Between brood types Between broods

1

2.67

6

71.13

Within broods Total

16 23

27,70 101.50

2.67

F test

F6j =4.44 P > 0.05 1 1 . 8 6 F6,16=6"86 P<0.01 1.73

Animal Behaviour, 33, 2

478

(this example was chosen since it uses the largest sample size). Of the eight broods, four were divided and four were not. This analysis and all the others performed on other data sets demonstrate that the within-brood variance is smaller than the betweenbroods variance and provide no evidence of a difference between those broods that are divided and those that are not.

(4) 'Two types of chick' hypothes& There are a number of ways in which the members of a brood could be divided into two types (e.g. male/female or large/small). Brood division may occur because it pays a particular parent to feed chicks of only one type, or a mixture of types. Alternatively, from the chick's point of view, it may be beneficial to be fed by a particular parent or to associate with siblings of a particular type. Snow (1958) noted that in the four cases in which he was subsequently able to determine the sex of in-chick blackbirds (Turdus merula), the fledglings had been of the opposite sex to their in-parent. A similar result holds for my robins: six out of seven sexed in-chicks were of the opposite sex to their in-parent. The exception was a male who was fed almost exclusively by his father. Although the sample is minute, the result is suggestive (binomial test, P~-0.062). Winglength is a rough guide to an adult robin's sex with males averaging larger than females (overlap between the sexes is about 40~). I have therefore compared the winglengths of chicks from the divided broods in Table III with the sex of their in-parent. As shown in Table VII, males had smaller in-chicks than did females and the result

still holds if data from the broods studied in less detail are included. Such an association between the winglength of a chick and the sex of its in-parent could arise in a number of ways. (a) The chick's winglength influences the likelihood of each parent feeding it because (i) it is advantagous for males to care for small chicks. There is evidence that male robins can carry larger prey loads than females can and this enables them to supply kilojoules to nestlings at a higher rate (Harper 1984). However it seems unlikely that small fledglings require more food in absolute tenons than do their larger siblings. Fledgling robins behave aggressively towards each other and it might be hypothesized that small chicks would benefit from the protection of their father. However not only do many female robins dominate their mates, but it is also dubious whether a parent could provide satisfactory protection to chicks when it is seldom near them. Adults have rarely been seen to intervene in aggression between their offspring. (ii) It is advantageous for females to care for large chicks. I can think of no reason why this should be so. (b) The sex of its in-parent influences the chick's winglength. There is no evidence to suggest that males feed fledglings at a low rate and that their in-chicks become somehow stunted. (c) The chick's winglength is not a cause or consequence of its in-parent's sex, but is correlated with some factor which is. One candidate for such a factor is chick sex. The observation that parents tend to care for

Table VII. Relationship between adult sex and chick winglength in divided broods Sex of parent Chickwinglength feeding chick (mm)median (range Mann-Whitney most frequently and sample size) test Broods studied Male 73 (71-75, N=7) in detail only Female 75 (74-77, N=5) No significant differences 72 (N= 1) between sexes All broods

U=2, P<0-01

Male 72.5 (70-76, N= 14) Female 75 (72-77, N= 11) U= 17, P<0.001 No significant difference 74 (72-76, N= 3) between sexes

479

Harper: Brood division in robins

young of the opposite sex could in theory be explained if males increase their reproductive success more by investing in daughters than in sons and/or females do best to invest in sons. There is evidence that in robins, as in most bird species (see Greenwood 1980), females are the dispersive sex (Harper 1984). Male philopatry might result in competition between a male and his adult sons and he may prefer to rear daughters who are less likely to compete with him. Alternatively, if males are capable of supplying more food to chicks than females, as was suggested above, it may pay them to put this investment into the dispersive sex. This strategy would be advantageous if the lifetime reproductive success of females was more strongly influenced by the level of parental investment (as a consequence of a higher average cost of dispersal for females) than that of males. It may be advantageous for both parents and offspring if each parent's in-chicks are as similar in size as possible. Chicks sharing the same in-parent compete more directly for feeds than do chicks with different in-parents. If a particular parent was, for example, feeding a large chick and a small chick there could be a risk that the larger chick could deprive its smaller sibling of food as a result of its despotic behaviour. Much of the aggression between siblings involves interference with each others' begging behaviour and attempts to interrupt the transfer of food from the parents. The reason that such competition is potentially more serious when it occurs between in-chicks of the same parent, rather than between chicks with different in-parents, is that only in the former case is the interference likely to result in the aggressor gaining food at its sibling's expense. One testable assumption of this hypothesis is that chicks of different sizes and/or sex should differ in competitive ability. Although the allocation of chicks between parents is correlated with chick size or sex, this relationship is not sufficient to account for brood division by itself. The fact that not all broods are divided suggests that this behaviour must have costs. One possible cost mentioned above is that the parents have to search for their in-chicks. Frequently parents carry food for several minutes before eating it themselves when they fail to locate an in-chick. Although the chicks' begging calls are one potential cue to their whereabouts (and possibly of their identity since I can, with practice, identify chicks by their calls; see also Smith &

Merkt 1980) they are frequently silent for long periods. The division of Early broods might inflict extra costs by reducing the female's ability to form a new clutch of eggs and by disrupting her incubation regime. It is of interest that of all the reports of brood division during incubation of which I am aware (Snow 1958; Smith 1978; this study) all have involved the female only feeding one chick. In summary, the functions of brood division remain unclear. However there is evidence that brood division is less likely to occur under conditions of food abundance. The fact that males tend to have smaller in-chicks than females may reflect a 'rule' the parents use to allocate the brood between them. Such a rule could be of the form 'care for chicks of the opposite sex to yourself'. A rule of allocation may be one important factor involved in the observed stability of brood division. If the parents were very good at discriminating between chicks on the basis of size or sex, for example, there would be no need to invoke individual recognition to explain brood division. In some species there is evidence that early experience of relatives can have long term influences on development, e.g. upon mate choice (Bateson 1978). It is therefore worth bearing in mind that a tendency for chicks to form associations with the parent of the opposite sex (for whatever reason it occurs) may have long-term consequences. ACKNOWLEDGMENTS I thank S. M. Walters and P. Oriss for permission to study the robins in the Cambridge University Botanic Garden, the SERC and Gonville and Caius College for financial support, J. D. Major for typing an earlier draft and N. B Davies, M. A. Elgar and two anonymous referees for their comments upon it. REFERENCES Bateson, P. 1978. Sexual imprinting and optimal outbreeding. Nature, Lond., 273, 659-660. East, M. 1981. Aspects of courtship and parental care of the European robin, Erithaeus rubecula. Ornis Scand., 12, 230-239. Grant, P. R. & Grant, B. R. 1980. The breeding and feeding characteristics of Darwin's finches on Isla Genovesa, Galapagos. Ecol. Monogr., 50, 381-410. Greenwood, P. J. 1980. Mating systems, philopatry and dispersal in birds and mammals, Anim. Behav, 28, 1140 1162.

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Hailman, J. P. 1978. Recent literature: Behavior, 16. Bird Banding, 49, 376. Hann, H. W. 1937. Life history of the ovenbird in Southern Michigan. Wilson Bull., 49, 145-237. Harper, D. G. C. 1984. The economics of foraging and territoriality in the robin Erithacus rubecula. Ph.D. thesis, University of Cambridge. Hinde, R. A. 1977. Mother-infant separation and the nature of inter-individual relationships: experiments with rhesus monkeys. Proc. R. Soc. Lond. Ser. B, 196, 2~50. Hinde, R. A. 1979. Towards Understanding Relationships. London: Academic Press. Hinde, R. A. & Atkinson, S. 1970. Assessing the roles of social partners in maintaining mutual proximity, as exemplified b y mother-infant relationships in monkeys. Anim. Behav., 18, 169-176. Lack, D. 1943. The Life of the Robin. London: Witherby. Nolan, V. 1978. Behavior and ecology of the prairie warbler. Am. Ornithol. Union Monogr., 14, 1-595. Portal, M. 1924. Breeding habits of the red-legged partridge. Br. Birds, 17, 315-316.

Siegel, S. 1956. Non-parametric Statistics for the Behavioral Sciences. New York: McGraw-Hill. Simmons, K. E. L. 1974. Adaptations in the reproductive biology of the great crested grebe. Br. Birds, 67, 413-437. Smith, J. N. M. 1978. Division of labour by song sparrows feeding fledged young. Can. J. Zool., 56, 187-191. Smith, J. N. M. & Merkt, J. R. 1980. Development and stability of single-parent family units in the song sparrow. Can. J. Zool., 58, 1869-1875. Snow, D. W. 1958. A Study of Blackbirds. London: George Allen & Unwin. Sokal, R. R. & Rohlf, F. J. 1969. Biometry. San Francisco: W. H. Freeman. Williamson, K. 1946. Field notes on the breeding biology of the whimbrel, Numenius phaeopus (Linnaeus). Northw. Nat., 21, 167-184.

(Received 3 June 1983; revised 16 January 1984; MS. number: 2388)