Pairing strategies and mate choice in female robins Erithacus rubecula

Anim. Behav., 1985, 33, 862-875

Pairing strategies and mate choice in female robins Erithacus rubecula D. G. C. H A R P E R *

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

Abstract. Female European robins (Erithacus rubecula) adopted three different pairing strategies. These were, in order of frequency: moving on to a male's territory; fusing her territory with that of a neighbouring male; and being joined by a male on her territory. Although females were not free to choose between strategies during a particular season, individuals frequently changed strategy between different years. Their behaviour suggested that they were exercising mate choice, although the scope for such choice was limited by a strong tendency for a female to pair in areas where she had lived previously (her 'Familiar Areas'). Males with large territories were more likely to pair and tended to pair earlier than those defending small territories. Female pairing strategy was also correlated with the area of their own territory. Although it is considered likely that some unidentified confounding variable was responsible for at least part of these relationships, possible causal explanations involving territory size are discussed. These include mate choice and a random settlement model. However the simplest explanation for the advantage enjoyed by males on large territories is that their territories were more likely to overlap with females' Familiar Areas.

It has become axiomatic in recent studies of animal behaviour that the individuals within a population differ in their attributes. These differences may have important consequences for the patterns of behaviour adopted by each individual (e.g. Dunbar 1982). Theoreticians have produced a variety of reasons for expecting animals to examine the attributes of another individual before copulating with it (see Halliday 1983 for a discussion of the degree to which these expectations are fulfilled). These reasons apply with particular force to females since their lifetime reproductive success will generally be more strongly influenced by the 'quality' rather than by the quantity of mates that they copulate with. The quality of a male to a female might be considered to depend on a range of factors from the genotype of the sperm received to the nature of any paternal care the resultant zygote receives (including utilization of resources defended by the male). Mate choice (for entry into recent literature see chapters in Bateson 1983) appears to be one strategy by which females can attempt to maximize the quality of each copulation (see Wasser 1983 for reproductive competition between females as another). In this paper I describe three different pairing * Present address: Edward Grey Institute, Department of Zoology, South Parks Road, Oxford, OXI 3PS, U.K.

strategies adopted by female European robins

Erithacus rubecula and investigate possible reasons for the choice between strategies made by individuals. My use of the word 'strategy' is not intended to imply anything about the relative benefits of these behaviours, nor to exclude the possiblity that females were employing a single conditional strategy. Evidence that females exercise mate choice is assessed, with particular attention to the possible constraints that are placed on them by the phenomena of partial migration and site fidelity. Robins are territorial for most of their adult lives. During the breeding season a male and female share a joint territory, but during the winter, members of both sexes defend individual territories. In north-western Europe, robins are partial migrants; most males remain on the same site for all of their adult lives but the majority of females are only summer visitors to their breedig sites (Burkitt 1924, 1925a, b, 1926, 1927). I shall refer to individuals that do not breed and winter at the same location as Migrants (following Lack 1943) to distinguish them from Resident individuals. Migrant females frequently return to the same breeding site in successive years (Burkitt 1924, 1925a, b, 1926, 1927; Lack 1943); such site fidelity will have inevitable consequences for female pairing behaviour.

862

Harper. Pairing in robins METHODS

These data were collected in the Cambridge University Botanic Garden during the springs of 1981 through 1983. The Botanic Garden is an area of about 16 ha of mature parkland situated in the suburbs of Cambridge. Individuals were marked with unique colour-ring combinations. The study site was visited thoughout most of the daylight period from early January to early July. It was exceedingly unusual for me not to see all of the individuals living on the study site during the course of the day. Observed dates of pairing were considered to be accurate to within 24 h. All dates are expressed relative to 1 January which was coded as day 1. The behaviour of a newly-formed pair was characteristic (see Results) and a pair was defined as being established on the first day that the male and female shared the same territory. Since there was a significant variation in pairing date between years (see Results) pairing dates were standardized relative to the median pairing date for that year, which was coded as day 0; a standardized pairing date of - 6 refers to a pairing that occurred 6 days before the population median. Territories were plotted on maps (at scales of 1:2200 and 1:750) using records of boundary disputes and song posts. The areas of the territories was measured from these maps using a Houston Hipad Digitizer and are quoted to the nearest 100 m:. The frequency of censuses of the entire study area provided sufficient data to monitor changes in territory size on a weekly basis. I shall make particular reference to the territory areas recorded at two specific points during the annual cycle. The first of these is the Pre-pairing Territory Area, which was recorded for all Resident individuals during the calendar week prior to the first pair forming (this measure was an excellent predictor of individuals' territory sizes until they paired). Secondly I shall refer to Breeding Territory Areas which were recorded for all pairs during the calendar week in which the first eggs were laid in the population (this measure was strongly correlated with the territory sizes of pairs throughout the breeding season). In order to investigate site fidelity I have used the term Familiar Area to denote the extent of an individual's previous home range. In this paper I shall distinguish between Summer and Winter Familiar Areas. The former were those areas where an individual had lived during the breeding season and/or moult period, while the

863

latter were those it had defended outside the breeding season. For example, a female that had bred in the Garden in two successive years would have a Familiar Area comprising the two territories involved; there is no reason why this should be a single contiguous area. If a female paired on a territory that overlapped to any extent with her Familiar Area she was deemed to have paired on that Familiar Area. Statistics follow Siegel (1956).

RESULTS General Observations

A total of 92 pairs were observed, involving 62 females and 44 males. Pairs were formed between early January and mid-June with most pairs being formed by the end of February (the first clutches were not laid until late March or early April). There were small but significant variations in median pairing date between years (excluding all known re-pairings within a season: 1981, median=34, range 10-124, N : 1 6 ; 1982, median=30, range 18-110, N = 2 3 ; 1983, median=22, range 6 82, N = 24; Kruskal-Wallis H = 10.573, df= 2, P<0.01). All females in the population paired although several males failed to pair during a particular season. Of the 71 occasions on which a male was still present on the study site at the end of the pairing period, 14 involved males that had failed to obtain a mate at all. This gives a point estimate of 19-7% for the proportion of males failing to pair. The majority of pairs were formed on territories within the study area, although in three cases established pairs entered the Garden from outside and evicted unpaired males. The remaining 89 pairs were formed in three distinct ways: (a) the female moved on to the male's territory ( N = 69); (b) the female and male had been defending adjacent territories and fused them together ( N = 11); or (c) the male moved on to the female's territory (N= 9). Pairs brought about by different pairing strategies tended to be formed at different dates relative to the population median pairing date, although these differences were not large (see Table IV). Early pairs were more likely to have been formed by a male and female fusing their adjacent territories, while late pairs were more likely to have been formed by a male moving on to a female's territory.

Animal Behaviour, 33, 3

864

Table I. Pairing strategies involved in primary, replacement and secondary pair-bonds (see text) Male pair-bond Pairing strategy

Primary Replacement Secondary Primary Replacement

Female joined male Male joined female Female and male fused territories

51 9 11

14

4

58 6 11

11 3

Totals

71

14

4

75

14

Three different types of pair-bond could be distinguished. (a) Primary pair-bonds: formed with the first mate that the individual had paired with that season. (b) Replacement pair-bonds: formed following the loss of a mate during that season (involved 14 re-pairings by females and 14 by males). (c) Secondary pair-bonds: formed by individuals that already had a mate. The pairing dates and pairing strategies of these different types of pair-bond are summarized in Fig. 1 and Table I. It was inevitable that replacement and secondary pair-bonds tended to be formed later than primary pair-bonds.

0.6"

i

i

Female pair-bond

i

0.5" / \ 0.4" 0.3 0.2

Primary(N=63)

Pairing Behaviour Quantitative data on the behaviour of 38 pairs on the day of pair formation will be presented elsewhere.

Female joined male For previous accounts see Lack (1943) and East (1981). Initially the female continually approached the male, who generally retreated from her singing loudly. This repeated displacement of the male by the female usually developed into hectic 'chases' around the male's territory with both birds giving snatches of song; I shall refer to this behaviour as 'Song Following'. Both birds were aggressive to one another at this stage of pair formation and several cases could easily have been mistaken for protracted territorial disputes. The duration of this phase of pair formation seems to be extremely variable, ranging from a few hours to several days. As noted by East (1981) females frequently terminate bouts of Song Following by leaving the male's territory and typically interact with several males prior to pairing (see below).

2- o.1. 0.4

0.50.20.1 ~

Repl]cement(N=22) Secondary(N=4)

,/o

80 " " ~zo

Date(JanuaryI =1)

16o

zro

Figure 1. Pairing dates for primary, replacement and secondary pair-bonds (see text). Data for primary and replacement pair-bonds expressed as frequency distributions, while exact dates plotted for secondary ones.

Female and male fused territories These cases of pairing were characterized by low levels of aggression between the male and female. Song following was a conspicuous feature of pairing and it was striking that the female followed the male while they were on his old territory, whereas he followed her around her old territory. In nine cases the previous histories of the male and female were known. Six involved the re-pairing of mates of the previous year and another involved a father and his daughter. In all seven cases the previous season's breeding territory had been divided between the male and female, who were

Harper: Pairing in robins

865 -4O

Table II. Fates of pairs on study area 1981-1983 Fate

Number of cases (%)

Remained together until moult

37 (40)

Female vanished Female deserted mate Female died

13 (14) 21 (23) 12 (13)

Male vanished Male deserted mate Male died

2 (2) 1 (1) 2 (2)

Pair evicted

4 (4)

sometimes seen interacting non-aggressively during the winter.

Male joined female These cases of pair formation started with a phase of extreme aggression between the future mates which I could not distinguish from attempts by intruders to evict territory owners. The female began to sing less frequently and in an increasingly small area of her territory. Then her behaviour would abruptly switch to Song Following.

Fates of Pairs Table II summarizes the fates of 92 pairs recorded during this study. Nearly a third of the pairs (31.5%) did not breed together. Female mortality during the period covered by Table II was significantlyhigher than that suffered by males (binomial test, P < 0.01). This difference appeared to be related to the costs of incubation, which were not shared by the male, since seven of the 12 hens that were found dead had definitely been killed while on the nest. Between 23 and 37% of all pairs separated as a consequence of the female deserting her mate. In contrast, only one male deserted his mate. Most of the desertions that occurred after breeding had started involved pairs that were caring for fledged young (75%, N = 12) and some of these females initiated their moult immediately after desertion (possible reasons for their deserting broods in order to moult are discussed elsewhere; Harper 1984).

Re-pairing by Males Males that lost their mates became less likely to

9~ 07 0.6 t 0.5 0.4] >" 0.:3

~;

~

-50 0o_

20

0.2

0.1 0

40 80 120 160 Date lost mate (January 1 =1) Sample size:4 10 5 4 5 8 5 5 o

--

0

200

2

Figure 2. Probability that a male losing his mate re-paired (continuous line)and the length of time that it took him to do so if successful (medians and ranges) plotted against the date on which he lost his mate. The number of males losing their mates in each time period is indicated under the horizontal axis.

re-pair as the season progressed (Spearman rank correlation, rs=--0-928, N = 9 , P < 0'01) and the length of time it took them to do so (which varied from a few hours to 38 days) increased (Spearman rank correlation on raw data, r~ = + 0"678, N = 14, P<0.01). These trends (Fig. 2) presumably reflected a decrease in the availability of females that were willing to pair. It is interesting that the availability of such females seemed to decrease between days 80 and 100, which was the period in which egg-laying commenced in all 3 years of the study.

Re-pairing by Females In view of the surplus of unpaired males in the population it might be assumed that all females that lost their mates would be able to re-pair. However during each year of the study, I found a few females moulting much earlier than the rest of the female population. Two of these females had deserted males in the Garden and both were estimated to have initiated their moult within a week of deserting their mates (even though other females that deserted later in the season had re-paired and made another breeding attempt). Since they had moved out of the Garden after deserting their mates it is unclear whether these females 'decided' not to re-pair or whether males 'refused' to pair with them. The latter seems particularly unlikely; during the breeding season, unpaired males courted all of the females that they encountered and one unpaired male even suspended his primary moult to take advantage of an

866

Animal Behaviour, 33, 3

unusually late opportunity to pair (Harper, in press). At least 16 of the 26 females separated from their mates before the end of the breeding season re-paired (for two exceptions see above; the other eight left the study area). The interval between separation and re-pairing was usually less than 2 days, although one female wandered about for 11 days before re-pairing. Some females were quick to exploit new opportunities to re-pair by deserting their previous mates. One striking example was provided when a paired female was accidently shut in a greenhouse. Within 2 h another female had moved 150 m from her previous mate's territory and was Song Following the trapped female's mate. In another instance a female transferred to a neighbouring male within 7 h of his first mate being killed by a cat. Both of these females had moved from territories that were contiguous with the territories of unpaired males that had been seen courting them. The fact that, although they had not responded to these advances, they re-paired within hours of another male becoming available for pairing is strong evidence in favour of the hypothesis of mate choice. Residents and Migrants Table III compares the pairing histories of Residents and Migrants of both sexes. The majority of pairing males were Residents (77.0~, N = 74), but less than a third of females had wintered on the study site (29.5~, N = 7 8 ; X2=29-627, df=l, P < 0-001). The majority of resident females (63-0~o, N = 2 7 ) paired on their own territories, but the remainder deserted their territories without being evicted. Out of a total of 16 males that vacated their territories during the pairing period only three deserted them without being evicted (compared with females: Fisher exact test, P < 0.05). Nine of the evicted males promptly vanished, but the other seven males that had vacated their winter territories (four evicted, three voluntarily) wandered around the study site interacting with females and, although none paired in the Garden, at least one of them succeeded in pairing nearby (pairing strategy unknown). The behaviour of these wandering ex-Resident males closely resembled that of 14 unpaired Migrant males that entered the study population during the spring. Nine of these Migrant males paired by joining unpaired females on their territories, while the remaining five estab-

Table IlL Pairing histories of Residents and Migrants of both sexes Stayed on winter territory Vacated winter territory Sex Residents Male Female Migrants Male Female

Failed Failed Left to pair Paired to pair Paired Garden 14 0

57 17

0 0

0 6

0 0

17 55

3 4

Birds that were evicted prior to pairing have been excluded.

lished their own territories either by evicting established birds ( N = 4) or replacing a predated male (N = 1). All five of these males had made unsuccessful attempts to pair with unpaired Resident females before establishing their own territories. Only two Migrant females ( N = 55) established territories in the Garden after their arrival. These territories were defended for between 4 and 9 days until the female moved on to a male's territory. Both females sang strongly in defence of these territories and it is interesting that they had the longest female wing-lengths recorded during the study (76'5 and 78'0 mm compared with: female median=72.5, range 69-78, N=136, male median= 74.0, range 70-78-5, N = 169). If all pairings are considered, regardless of whether they involved re-pairing individuals or not, the pairing dates of Resident females tended to be slightly in advance of those of Migrant females, although not significantly so (standardized pairing dates: Residents, median = - 4, range - 24 to + 93, N = 2 5 ; Migrants, m e d i a n = + 5 , range - 1 6 to + 126, N = 64; Mann-Whitney U = 676, P < 0.10). This form of analysis inevitably exaggerates any genuine difference between the average pairing dates of the two classes of females. The central problem is that Resident females that moved between territories to re-pair were likely to leave the Garden while all individuals entering to re-pair would be classified as Migrants. There is no entirely satisfactory method of dealing with this problem. If all known re-pairings are excluded from the analysis the difference in pairing date between Resident and Migrant females is reduced (Residents,

Harper: Pairing in robins m e d i a n = - 6 , range - 2 4 to +90, N = 2 3 ; Migrants, m e d i a n = - 4 , range --16 to +80, N = 40; Mann-Whitney U = 399' 5, P > 0" 10). However if the distributions of pairing dates of males and females are not identical, this restricted analysis will also be biased; the extent of this bias cannot be estimated since the pairing histories of Migrant females were incompletely known.

Individual Consistency Individuals did not adopt the same pairing strategies throughout their lives. For example, all of the five males pairing in three successive years adopted at least two different pairing strategies. It is not surprising that females frequently changed pairing strategy since there was no tendency for females to adopt the same wintering strategy in successive years (pairing strategy correlated with wintering strategy, Table III). About half (43%, N = 28) of the females for which the necessary data were available changed their winter strategy during their lives (Biebach 1983 has reported a strong genetic influence on migratory tendencies in robins). There was no discernible direction to these changes and no evidence that strategies were age-dependent.

867

Territory Size and Pairing The males that failed to pair were not a random subset of the males in the population and had significantly smaller territories than average (Table IV; comparing males that did not pair wth successful males: Mann-Whitney U=73.5, P<0-001). The date on which males were joined on their territories by females was negatively correlated with the male's territory size; in other words, males with small territories were not only less likely to pair than those with large territories but they were also likely to pair later (Spearman rank correlation coefficients: 1981, rs=--0-711, N = l l , P<0.05; 1982, rs=--0-724, N = 1 9 , P<0"01; 1983, rs=--0'537, N = 15, P<0'05). Although the sample size was very small, it is interesting that the three males to vacate their territories without being evicted had small teritories (Table IV). The pairing strategy adopted by Resident females was related to the area of their winter territories (Table IV). Females that were joined on their winter territories by males had significantly larger winter territories than those females that either vacated their territories or fused them with that of a neighbouring male. Moreover the date at which females vacated their territories (relative to the median pairing date) was positively correlated

Table IV. Differencesin pre-pairing Territory Area and pairing date between robins employing different pairing strategies Territory area (m2 x I0) Pairing strategy

Male

Female joined 29 (11-63; 45) male Male joined -female Female and male 27 (10-35; 11) fused territories

Female 22 (12-28; 10)

0 (--22 to +80; 45)

30 (27-38; 6)

+5 (+ 1 to + 19; 6)

24 (11-30; 11)

- 6 ( - 2 4 to +90; 11)

Mann-Whitney Kruskal-Wallis U= 183 P>0-10 H= 11.956 P<0.01 Male vacated territory Male failing to pair

Pairing date

Kruskal-Wallis H=7.230 P<0.05

14 (9-16; 3) 13 (8-23; 14)

Data are presented as medians with range and sample size in parentheses. Pairing dates are expressed in days relative to the population median in the year in question.

Animal Behaviour, 33, 3

868 8-

with their Pre-pairing Territory Area ( S p e a r m a n r a n k c o r r e l a t i o n , rs = + 0.851, N = l 0, P < 0'0 l).

7-

Territory Size and Breeding Success

o 6"5 I1)

54I

"6

Z

s!

O0

2,

9

1. 0

00

IO 9

9

~ 0

lb

9

zo

00

9

~.

~.,

9

~0 Q

~., so

40

50

do

7'o

Pre-pairing territory area x 10 m e Figure 3. Female reproductive success, measured as number of chicks reaching independence, plotted against the area of the territory on which she paired.

Female breeding success was positively correlated with the area of the territory on which she paired (Fig. 3). A n analysis of factors correlating with reproductive success will be presented elsewhere. F o r present purposes it is sufficient to note t h a t the relationship s h o w n in Fig, 3 reflects lower mortality of recently-fledged young o n large territories (Breeding Territory A r e a positively correlated with t h a t at pairing; r s = +0"761, N = 3 4 , P < 0'01) a n d t h a t the analysis revealed n o independent relationships between pairing strategy a n d reproductive success.

Site Fidelity As d e m o n s t r a t e d in T a b l e V, females tended to pair o n territories overlapping with their S u m m e r Familiar Areas, whether they were yearlings or

Table V. Previous histories of females pairing in the Botanic Garden in 1982 and 1983 Previous history

1982

1983

2 (2S) 5 (3S, 2W) 2 (2W)

7 (7S) 2 (IS, lW)

2 (2S) 1 (1S) 4 (4S) 2

5 (3S) 1 (1S) 3 (2S)

Residents Had bred before Yearling Unknown background* Migrants Had bred before Had brought fledged young into area Had held juvenile territory Had been non-territorial juvenile Had moulted in area Had held winter territory a year ago Not ringed

1 11

8

Totals

30

27

1

The number of cases in each year is given with the number of cases in which the female returned to part of her Summer or Winter Familiar Areas (see text) in parentheses (S: Summer; W: Winter). The categories in the left-hand column have been made mutually exclusive. For example, a female that had held both a juvenile and a winter territory is entered as a Resident even though her Summer Familiar Area consisted of her juvenile territory. Similarly, if the territory on which a female paired was on both her Summer and Winter Familiar Areas it is recorded under the former only. * An additional three Residents with unknown backgrounds left the study area before pairing,

Harper: Pairing in robins adults (63~ and 80~o of cases respectively; Fisher exact test P > 0-10) and whether they were Residents or Migrants (81~o and 70~o respectively; Fisher exact test, P>0.10). An additional five Resident females paired upon their Winter Familiar areas (i.e. their winter territories). None of these Familiar Areas covered more than 10~ of the Garden (median=5400 m 2, range 1200-13100, N = 28; the Garden covered about 155 000 m2). The proportion of females that had remained in the Garden until the moult that bred within the confines of the study area in the following year was similar for Residents and Migrants (pooling data: Residents 69~, N = 1 3 ; Migrants 58~, N = 12; Fisher exact test, P>0.10). However only one of the females that had left the study area (alive) between the start of the pairing period and the end of the breeding season, returned to breed in a subsequent year (6~o, N = 16; Fisher exact test, P<0.01). It is interesting to note that three of the six Migrant females that failed to return to part of their Familiar Area may have been prevented from doing so by the fact that there were no unpaired males available in these areas when they returned. Although unpaired and paired females were frequently seen fighting, there was only one instance in which a paired female was evicted. This general inability (or unwillingness) of unpaired females to displace established birds made it inevitable that some females paired away from their Familar Areas. Only three Resident females whose previous histories were known failed to pair on their Summer Familiar Areas. All of these cases involved females whose winter territory was not contiguous with her Summer Familiar Areas. In contrast to Migrant females, Residents ought to be able to prevent themselves from being pre-empted by other females and would be expected to pair on their Summer Familiar Areas 'if they wanted to'. The failure of these three females to do so emphasizes that there were other factors influencing a female's choice of mate. Only about a third of the females pairing on their Summer Familiar Areas did so with a former mate (35~o, N = 26), suggesting that it is more likely that cases of re-pairing were consequences of site fidelity, rather than the reverse. Six of the nine females re-pairing with their former mates were Residents and three were Migrants. An additional three females (one Resident, two Migrants) did not re-pair with their former mates even though they

869

22. 21

,~ ~ ~ " tL

20 19 18 17 15 14 Unpaired 0

1 2

5

4

5

6

7

8

9 10 11 Paired

Days since first seen wandering

Figure 4. Female weight plotted against length of time spent wandering before pairing. Solid linesjoin retraps of the same individual. At the left and right the median weights (with 95~o confidence limits) of unpaired and paired femalesare given. All birds were weighed within 2 h of sunrise in January or February.

had the opportunity, Similarly Lack (1939, 1943) recorded that six out of nine females (five out of five Residents and one out of four Migrants), with the opportunity to pair with the same male in successive years, did so. Pooling our data suggests that Resident females are more likely to re-pair with their former mate than Migrant females (Fisher exact test, P < 0.05). Costs of Wandering Wandering robins were nearly always attacked by conspecifics of the same sex and sometimes by members of the opposite sex. One wandering female was killed by a male and a wandering male was found dying from head injuries and being harried by a territorial male. Retraps of females suggested that they lost weight while wandering (Fig. 4; rs = - 0' 526, N = 24, P < 0' 01). T he alternative explanation that light females were forced to wander longer before pairing is unlikely, since no territorial female (paired or unpaired) was ever caught with a weight of less than 17 g except in extreme weather conditions (N > 500).

Bigamy At least three of the four females that became the secondary mates of bigamous males had initially been paired monogamously to another male. The bigamous males all had large territories (range 5200-7700 m 2compared with other Breeding Terri-

Animal Behaviour, 33, 3

870

tories: median = 5500 m 2, range 2500-8300, N = 59; Mann-Whitney U = 84, P < 0.01). It may be important for their territories to be relatively large since the females divided the available area between them, each female excluding the other from its own half. Quantitative data on the relationships between adults and offspring in bigamous trios will be reported elsewhere (e.g. Harper 1985).

DISCUSSION There are a variety of hypotheses that could be advanced to explain the observed correlations between territory area and the type of pairing strategy that an individual adopted, and how successful that strategy was. For example, consider the observation that males with large territories pair earlier in the season than those with small territories. There are three different types of hypothesis which might explain this correlation. (1) Pairing was random in the sense that neither sex exercised mate choice; males on larger territories were more likely to encounter unpaired females. The particular form of this hypothesis that I have chosen to discuss is a model of random female settlement. (2) Pairing was non-random in the sense that males on larger territories were available for pairing earlier in the season. (3) Pairing was non-random in the sense that females chose males with larger territories. In all three cases, there is a strong possibility that the correlation was not causal and was confounded by some other attribute of the male or his territory. Therefore, before evaluating the different types of hypothesis, it is worth considering the nature of potentially confounding variables.

Confounding Variables The most obvious set of confounding variables would be male attributes that influenced competitive ability, for instance age and body size.

Age There were no significant differences between the territory sizes or the pairing success of adult and yearling males (Table VI).

Body size Tarsus length was used as a crude measure of body size (method per Svennson 1975). There was

Table VI. Pre-pairing Territory Areas and pairing success for yearling and adult males Adults

Yearlings

P

Pre-pairing Territory Areas (m2 x 10): median (range, N) 1982 30(15-49; 11) 22(11-37; 10) P>0.10 1983 28 (10-52; 14) 25 (14-49; 9) P>0.10 Total 29 (10-52; 25) 25 (11-49; 19) P>0.10 Percentage failing to pair 1982 18.2~ 1983 21.4% Total 20.0%

22.2% 20.0% 21-1%

P>0.10 P>0.10 P>0.10

No data are available for 1981. Table VII. Spearman rank correlation coefficients (rs) between Pre-pairing Territory Area and tarsus-length Sample

r

N

P

Males 1982 +0.344 28 P<0.05 1983 +0.402 26 P<0.05 Females 1982-1983 +0-411 18 P<0.05

no evidence that tarsus length changed after about 15 days post-hatching. Table VII demonstrates that Pre-pairing Territory Area was positively correlated with tarsus length for both sexes in each of the years (1982-1983) for which data were available. In the case of females, I have had to pool data using the mean territory size for females present in both years. Wing-length is not as good a measure of body size since there is a weak tendency for it to increase with age. However the above relationships held in all 3 years of the study if wing-length was used instead. Wing-length was therefore used in a partial correlation analysis to test whether holding male 'body-size' constant abolished the observed relationship between the territory size and pairing date of males that were joined by a female, since this enabled data from all 3 years to be used (Table VIII). Unfortunately the sampling distribution of partial z is not known (Siegel 1956) and therefore significance levels cannot be calculated. However the fact that only small percentage reductions were observed when winglength was controlled for suggests that it was not an important confounding variable. Note that when territory size was held constant, the observed

Harper: Pairing in robins

871

Table Vlll. Kendall rank correlation coefficients between Pre-pairing Territory Size (T), wing-length (W) and pairing date (P)

Simple correlations Year N

T,P

1981 11 -0.514 1982 19 -0.469 1983 15 -0.505

T,W

W,P

+0.321 -0.171 +0.257 -0.168 +0.427 -0.194

Partial correlations T,P.W

W,P.T

-0.492 -0.007 --0.447 +0.056 --0.476 +0.028

Data are only for males that paired by being joined by female. correlations between wing-length and pairing date (which were not statistically significant) were considerably reduced. Similar results held if tarsuslength was controlled. Although it can be demonstrated that specific variables, such as age or measures of body size, were not confounding the observed correlations, it is impossible to rule out the possibility that some unspecified variable was doing so. Unfortunately I could think of no method of experimentally manipulating territory size independently of other variables such as food density, which would be the only way of demonstrating that the observed relationships were causal.

Hypothesis 1: Random Female Settlement It is possible that females chose to pair at a particular location without any reference to the attributes of the local males and that the advantage enjoyed by males with larger territories was merely a consequence of their territories being more likely to contain the location chosen by the female. A n obvious candidate for such a location would be the

female's Familiar Area. The same result would also obtain if the females fell out of the sky at random and paired with the nearest unpaired male. Studies on artic skuas, Stercorarius parasiticus, provide an interesting parallel to my robins, with males on large territories pairing earlier than those on small territories and females exhibiting site fidelity (O'Donald 1983). Davis & O ' D o n a l d (1976, see also O ' D o n a l d 1977) devised a simple probabilistic model, based on assumptions of the type outlined above, which gave superficially good fits to their data on pairing in the arctic skua. Unfortunately the model is not directly applicable to my data and a rather naive test had to be conducted by ignoring all individuals that did not pair by the female joining the male, and all cases of re-pairing. Table IX shows one result of this test; it demonstrates that the expected and observed numbers of males, with territories of different sizes, that failed to pair were similar (Kolmogorov-Smirnov test, D = 0.24, P > 0.10). Note that the ability of some males to re-pair means that this crude test underestimates the real discrepancy between the predictions and the data. It should, however, caution against

Table IX. Comparison of observed proportions of males with territories of different size classes that failed to pair and the predictions of a model described in the text Male Pre-pairing Territory Area (m2 x 10) <19

20-29 30-39 40-49

>50

Total number 22 16 14 5 Observed not to pair 13 1 0 0 Predicted not to pair 9.24 2-98 1-56 0 - 2 0

2 0 0.02

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Animal Behaviour, 33, 3

elaborate hypotheses involving active female choice of large territories.

Hypothesis 2: Male Availability

The earliest pairs were formed when the availability of the invertebrates preyed on by the robins was at its lowest (results of analysis of robin faeces and pitfall trapping). As will be discussed elsewhere, individuals on small territories had more difficulty in maintaining their body-weight than individuals defending large territories and this may explain why males on small territories initially failed to court wandering females but drove them away. Experimental manipulation of the food supply on the territories of unpaired males demonstrated that this hypothesis was not sufficient to explain the lower pairing success of males with small territories since, although the behaviour of males towards females could be changed by increased food availability, the responses of females to the males was not altered (Harper 1984). Moreover the intolerance of these males was short-lived (presumably as a reflection of the dramatic increases in food availability that were recorded during the spring) and could not have accounted for the fact that males with small territories remained unlikely to pair throughout the breeding period.

Hypothesis 3: Mate Choice

Much of the data could be explained by invoking mate choice by females. Females were in a position to exercise such choice since there was a surplus of males in the population and most females encountered several males before pairing. Note that Resident females that remained on their winter territories had fewer options than wandering females (most had only two male neighbours, with a range of 1-4, and there were few wandering males). Although three females were observed to interact with between 10 and 15 males, the degree of site fidelity shown by many females suggests that their choice is rather more restricted than such figures imply. Female mate choice on the basis of male territory size (or some correlate) would not be a tenable hypothesis if females were unable to assess territory size or if their fitness was negatively correlated with the size of the territory chosen. The observation that females on large territories enjoyed higher

reproductive success than those on small territories (Fig. 3) is strong evidence against the latter proposition (although imperfect since it involves interand not intra-individualcomparisons). Although it is impossible to provide direct evidence about the ability of females to assess territory size, it may be noted that Song Following is exactly the kind of behaviour that might be predicted if robins were attempting to assess the territory size of a potential mate. If females really were attempting to maximize the size of breeding territory that they obtained, it would be predicted that nearly all Resident females should pair by fusing their territories with that of a neighbouring male (see Table IV). Despite the fact that all Resident females had between one and four male neighbours (median = 2) under half of them (41~, N = 27) paired in this manner. The observation that these cases often involved re-pairing of mates from previous seasons suggests that there may be constraints on the use of this pairing strategy.

Familiar Area and Mate Choice

Table X investigates the extent to which the observed patterns of pairing could be explained by

Table X. Mate choice by females that had Summer Familiar Areas in the Botanic Garden in 1982 and 1983

Number of unpaired males on Summer Familiar Area Number pairing on Largest territory on Summer Familiar Area Another territory on Summer Familiar Area A larger territory than available on Summer Familiar Area* A smaller territory than available on Summer Familiar Area

0 I 2 3 4 5 6 7 4661 342 21 1

1 1

Territories were consideredto be availableif they were held by an unpaired male. * Includes three femalesthat paired by territory fusion away from their Summer Familar Area even though the latter contained unpaired males.

Harper: Pairing in robins

873

tories may have done better by 'staying put' rather than vacating their territories in order to 'look for' a high-quality male or territory. If territory area was an important component of territory quality, the balance of benefits for females on small territories may have favoured territory desertion. The second (non-exclusive) hypothesis is that 'quality' is not a single entity: what makes a robin good at territory defence might not make it good at incubating eggs, for example. It seems likely that the optimal phenotype for males and females differs and it is possible that females able to defend larger winter territories were not high-quality birds in other senses. The paradox would be resolved if there was a negative correlation between components of quality influencing winter territory size and those influencing seasonal reproductive success for females and not for males.

supposing that females paired with the male defending the largest territory on their Summer Familiar Area. If only females with a choice are considered, about half (57~o, N = 23) paired with the male that would be predicted under this hypothesis. This was significantly higher than would have been predicted if pairing was random with respect to territory size (Z2=5.27, df= 1, P < 0.05). There are two obvious types of explanation for the failure of females to show an absolute preference for the largest territory. First it seems likely that territory size was not the only factor influencing female mate choice, while secondly there could be constraints upon the mechanism by which females tended to pair on large territories. For instance if females were assessing each male's territory size (or some correlate) they might make errors of assessment or be limited as to how much information they could store.

Residents and Migrants Quality of Mates

It has been suggested that Migrant females are at a disadvantage compared with Residents because they will pair later as a consequence of having to move back into breeding habitats (Lack 1943; East 1981). If Resident and Migrant females 'prefer' the same male attributes, Migrants run the risk of pairing with less-preferred males. Table XI demonstrates that the difference in average pairing dates varies considerably between populations. One explanation is that the distance travelled by Migrants is variable; note that latitude does not seem to influence the difference in pairing dates (contra Lack 1943). The observations of wandering birds being ser-

It might be expected that 'high-quality' individuals of both sexes tend to defend larger territories than 'low-quality' birds. If this is correct, the data contain an interesting paradox: high-quality (large territory) females tended to pair with lowquality (small territory) males. This resulted from the tendencies of females from large territories to either pair with wandering males (Table IV) or to move off their winter territories later than other individuals. There are two possible methods of reconciling this apparent paradox with the mate choice hypothesis. First, if females benefited from breeding on Familiar Areas, those on large terri-

Table XI. Relative pairing dates of Resident and Migrant femalesin four studies of pairing in robins Median Pairing Date Study

Latitude

Habitat

Burkitt (1924-1927) Jackson (1958) Present study Lack (1943)

54~19'

Rural

53015, 52011' 50~ '

Residents Migrants

January March (6) (16) Suburban llJanuary 10January (11) (10) Suburban 26 January 2 February (25) (64) Rural January February (11) (22)

Sample sizes are given in parentheses.

Mann-Whitney U-test U= 0 P< 0.001 U=45 P>0.10 U=676 P > 0.05 U= 44 P < 0.01

874

Animal Behaviour, 33, 3

iously injured or killed, and of weight loss among wandering females, suggest that moving between territories is costly. All Migrants have to pay these costs, but most Residents in this study did not move at all. Moreover all six Resident females that vacated their territories and paired in the Garden, did so on the same day (N = 6).

Generality of Results Lack (1940) found no evidence that territory size influenced pairing success. In the Botanic Garden, territory size was an important component of territory quality, being correlated with the ability of individuals to maintain body weight during the winter and to share their territory with their mate (Harper 1984). It was also likely to have been correlated with individual 'quality'. If territory size was not so closely correlated with such factors in Lack's study, no relationship between territory size and pairing success would be expected if either the male availability or the mate choice hypotheses was correct. However this excuse for the difference between studies would be an unlikely explanation if the type of r a n d o m female settlement model posited above is an important reason for the correlations observed in this study. It would be interesting if future studies of robin pairing included measures of territory quality.

Site Fidelity The marked site fidelity of some Migrant robins has been recorded in previous studies in both breeding (Burkitt 1924, 1925a, b, 1926, 1927, Lack 1943) and wintering sites (e.g. Marples 1936; Bannerman & Bannerman 1971; Herrera & Rodriguez 1979; Finlayson 1980). Similar site fidelity is known to be a feature of the natural history of migrant birds ranging from blue grouse Dendropagus obscurus (Bendell & Elliott 1967) to hobbies Falco subbuteo (e.g. Cramp & Simmons 1980). Birds exhibiting site fidelity are either responding to some important benefit of previous experience of a site or displaying an incredible lack of imagination. There are virtually no quantitative field data on the possible advantages of previous experience of a site. This dearth of information is particularly unfortunate in view of the evidence for considerable intraspecific variation in the degree of site fidelity; compare for example the data on breeding site fidelity in the masked booby, Sula dactylatra, presented by Kepler (1969) and Nelson (1978).

ACKNOWLEDGMENTS These observations were made during a study supervised by N. B. Davies and financed by SERC and Gonville and Caius College, Cambridge. S. M. Walters and P. Oriss gave me permission to watch birds in the Botanic Garden. The staff of the Botanic Garden provided invaluable assistance. Many members of the public reported sightings of robins that had left the study area; I hope that they will soon discover where most of the Migrants go! J. Watson measured some of the territory areas from maps. A previous draft was improved by Nick Davies and two anonymous referees. I thank them all.

REFERENCES Bannerman, D. A. & Bannerman, W. M. 1971. Handbook of the Birds o f Cyprus and Migrants of the Middle East.

Edinburgh: Oliver & Boyd. Bateson, P. 1983. Mate Choice. Cambridge: Cambridge University Press. Bendell, J. F. & Elliott, P. W. 1967. Behavior and the Regulation o f Numbers in Blue Grouse. Canadian Wildlife Report Series No. 4. Ottawa: Department of

Indian Affairs and Northern Development. Biebach, H. 1983. Genetic determination of partial migration in the European robin. Auk, 100, 601 606. Burkitt, J. P. 1924. A study of the robin by means of marked birds. Br. Birds, 17, 294-303. Burkitt, J. P. 1925a. A study of the robin by means of marked birds (second paper). Br. Birds, 18, 97-103. Burkitt, J. P. 1925b. A study of the robin by means of marked birds (third paper). Br. Birds, 18, 250-257. Burkitt, J. P. 1926. A study of the robin by means of marked birds (fourth paper) Br. Birds, 19, 120-124. Burkitt, J. P. 1927. A study of the robin by means of marked birds (fifth paper). Br. Birds, 20, 294-303. Cramp, S. & Simmons, K. E. L. 1980. Handbook of the Birds o f Europe, the Middle East and North Africa. Vol. II. Oxford: Oxford University Press.

Davis, J. W. F. & O'Donald, P. 1976. Territory size, breeding time and mating preference in the arctic skua. Nature, Lond., 260, 774-775. Dunbar, R. E M. 1982. Intraspecific variations in mating strategy. In: Perspectives in Ethology, Vol. 5 (Ed. by P. P. G. Bateson & P. H. Klopfer), pp. 385 431. New York: Plenum Press. East, M. 1981. Aspects of courtship feeding and parental care of the European robin Erithacus rubecula. Ornis Scand., 12, 230-239. Finlayson, J. C. 1980. The recurrence in winter quarters at Gibraltar of some scrub passerines. Ringing Migr., 3, 32-34. Halliday, T. R. 1983. The study of mate choice. In: Mate Choice (Ed. by P. Bateson), pp. 3-32. Cambridge: Cambridge University Press9

Harper. Pairing in robins Harper, D. G. C. 1984. The economics of foraging and territoriality in the European robin. Ph.D. thesis, University of Cambridge. Harper, D.G.C. 1985. Interactions between adult robins and chicks belonging to other pairs. Anim. Behav., 33, 876-884. Harper, D. G. C. In press. Moult interruption in passerines resident in Britain. Ringing Migr. Herrera, C. M. & Rodriguez, M. 1979. Year-to-year site constancy among three passerine species wintering at a southern Spanish locality. Ringing Migr., 2, 160. Jackson, R. D. 1958. A study of a population of robins, Erithaeus rubecula. Irish Nat. J., 12, 1-8. Kepler, C. 1969. The breeding biology of the blue-faced booby (Sula dactylatra personata) on Green Island, Kure. Publ. Nuttall Ornithol. Club, 8, 1-97. Lack, D. 1939. The behaviour of the robin. Part I. The life history with special reference to aggressive behaviour, sexual behaviour and territory. Proe. Zool. Sot., Ser.

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Marples, G. 1936. Some results of trapping and ringing. Br. Birds, 29, 22-25. Nelson, J. B. 1978. The Sulidae. Oxford: Oxford University Press. O'Donald, P. 1977. Sexual selection and the evolution of territoriality in birds. In: Lecture Notes in Biomathematics 19. Measuring Selection in Natural Populations (Ed. by F. B. Christiansen & T. M. French), pp. 113-129. Berlin: Springer-Verlag. O'Donald, P. 1983. The Arctic Skua. Cambridge: Cambridge University Press. Siegel, S. 1956. Nonparametrie Statistics for the Behavioral Sciences. New York: McGraw-Hill. Svensson, L. 1975. Identification Guide to European Passerines. Stockholm: Naturhistoriska Riksmuseet. Wasser, S. K. 1983. Reproductive competition and cooperation among female yellow baboons. In: Social Behavior of Female Vertebrates (Ed. by S. K. Wasser), pp. 349-390. New York: Academic Press.

A., 109, 169-200. Lack, D. 1940. The behaviour of the robin. Population changes over four years. Ibis, 82, 299-324. Lack, D. 1943. Life o f the Robin. London: Witherby.

(Received 15 February 1984; revised 4 June 1984," MS. number: 2487)