- Email: [email protected]
Do female pigeons trade pair copulations for protection?
ANIMAL BEHAVIOUR, 1998, 56, 235–241 Article No. ar980774
Do female pigeons trade pair copulations for protection? CLAIRE LOVELL-MANSBRIDGE & T. R. BIRKHEAD
Department of Animal and Plant Sciences, University of Sheffield (Received 1 August 1997; initial acceptance 16 September 1997; final acceptance 11 December 1997; MS. number: 5606)
ABSTRACT Male pigeons, Columba livia, employ intense mate guarding and frequent copulation apparently as strategies to ensure their paternity. The aim of this study was to investigate the benefits to females of mate guarding by males and frequent copulation. Field observations showed that females initiated the majority of copulations and females that solicited copulations more frequently were guarded more closely by their partner. Experimental removal of guarding male partners showed that: (1) unguarded, fertile females suffered increased harassment from extrapair males which reduced their foraging efficiency; and (2) unguarded, fertile females did not seek copulations with extrapair males. Various explanations for frequent pair copulation initiated by females are discussed and we conclude that female pigeons trade pair copulations for protection (mate guarding) against sexual harassment from other males.
In socially monogamous birds, the frequency with which pairs copulate prior to egg laying varies markedly across species (Birkhead et al. 1987). In a review of hypotheses proposed to explain this variation, Birkhead & Møller (1992) concluded that copulation frequency within pairs is best explained by the sperm devaluation hypothesis: copulations are more frequent in species where the risk of extrapair copulations is high because sperm from frequent pair copulations devalues the sperm of competing males. This is consistent with the known mechanism of sperm competition in birds (Birkhead et al. 1995; Colegrave et al. 1995). In many species, however, it is the female and not the male who initiates pair copulations (Birkhead & Møller 1992), so more recent studies have asked how females might benefit from repeated copulations with the same male (Petrie 1992; Hunter et al. 1993). Several hypotheses have been proposed to explain why females copulate at high frequency with their partner. (1) In species where parental care by males is important, females may encourage repeated copulations to assure their partner of his paternity. Males may be more likely to feed young if they have copulated with a female and thus are confident of their paternity (e.g. Burke et al. 1989; Davies et al. 1992; Westneat & Sherman 1993; Houston 1995). (2) Females may employ frequent copulation as a mate-guarding strategy, since males that copulate frequently with their partners may be less likely to mate with other females (Petrie 1992). For example, female starlings, Sturnus vulgaris, use copulation solicitations to
interrupt their males’ singing and thus prevent them from becoming polygynous (Eens & Pinxten 1995). (3) Multiple copulations may increase the likelihood of eggs being fertilized (Birkhead et al. 1987). However, as one or a few ejaculates usually contain enough sperm to fertilize all the eggs in a clutch (Birkhead et al. 1987), there is little evidence for this (Lake 1975; but see Adkins-Regan 1995). Frequent copulation is the primary paternity guard employed by many colonial breeding birds and birds of prey. In most other bird species, males guard their partner by close following during their fertile period (Birkhead et al. 1997). In many species frequent copulation and mate guarding appear to be alternatives (Møller & Birkhead 1991), but some species employ both paternity guards (e.g. Birkhead et al. 1988; Sheldon 1994). The benefits to males of guarding females have been demonstrated in studies where temporary removal of males has resulted in an increase in the number of extrapair copulations directed at their partner (e.g. Bjo ¨ rklund & Westman 1983; Møller 1987; Birkhead et al. 1989). However, observations on eider ducks, Somateria mollissima, ring doves, Streptopelia risoria, bar-headed geese, Anser indicus, and blue tits, Parus caeruleus, have shown that females may also benefit from mate guarding, as the close proximity of a pair male affords protection from the unwanted courtship of other males, and thus allows females to forage more efficiently (Ashcroft 1976; Lumpkin 1983; Lamprecht 1989; Kempenaers et al. 1995). Furthermore, Lumpkin (1983) suggested that female ring doves may actively manipulate mate guarding by males to extend the period over which they gain these benefits (see also Enquist et al. 1998).
Correspondence: T. R. Birkhead, Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, U.K. (email: [email protected]). 0003–3472/98/070235+07 $30.00/0
1998 The Association for the Study of Animal Behaviour
235
1998 The Association for the Study of Animal Behaviour
236 ANIMAL BEHAVIOUR, 56, 1
A previous study concluded that male feral pigeons, Columba livia, employ both frequent copulation and mate guarding as paternity guards (Lovell-Mansbridge 1995). Pigeons are colonial breeders and feed in flocks (Cramp 1986; Johnston 1992) and where they exist at high densities, aggressive competition for food and partners can occur (Murton et al. 1972; Johnston 1992). The high frequency of pair copulation and the intense mate guarding by males are consistent with sperm competition hypotheses as the temporal pattern of both behaviours closely matches the timing of the release of ova from the ovary (Lovell-Mansbridge 1995). However, as females of most bird species solicit copulations more often than males (Birkhead & Møller 1992), an explanation for the adaptive significance of frequent copulations for females is necessary. As pigeons forage and breed at high densities, and display intense paternity guards, we predicted that male removal experiments would increase the likelihood of extrapair copulation. Our aims in this study therefore were: (1) to determine why females initiate frequent copulations with their social partner; and (2) to determine how fertile female pigeons behave in the absence of their guarding partner.
METHODS Behavioural observations largely followed those in Lovell-Mansbridge (1995) but briefly were as follows. We observed 21 pairs of colour-ringed birds at a dovecote in Derbyshire, England, over three breeding seasons (1993–1995) from March until September, using focal group sampling (Altmann 1974). Each pair was observed for a meanSE of 22.733.8 h (range 4–50 h) between day 5 and day 0 (the day the first egg was laid). Observations began when the female of a pair was first located and lasted a minimum of 20 min for each pair; up to six pairs could be watched simultaneously. During each observation period, we recorded specific behaviours on a printed tick sheet. Behaviours relevant to this study were defined as follows. (1) Intrapair distance in metres, or if <1 m in centimetres. (2) Copulation initiation: the sequence of copulation begins when a bird begs for courtship feeding, by gentle pecking movements at the base of its partner’s bill (see also Fabricius & Jansson 1963). The female inserts her bill into that of the male, and he appears to regurgitate food; feeding is symbolic as food is rarely passed (Heinroth & Heinroth 1949). Courtship feeding is followed by copulation (Fabricius & Jansson 1963). The sex of the bird soliciting copulation by begging was recorded. (3) Copulation: the number of copulation attempts. (4) Moves followed: the number of moves of 10 m or more, initiated by a pair member, that were followed by the other pair member within 5 s. (5) Extrapair males: the number of other males within 10 m of the focal pair. (6) Duration of male courtship: male pigeons show a characteristic ‘bowing’ display towards females, in which
they ruffle their neck feathers and sweep their fanned tail along the ground whilst giving a display call (Fabricius & Jansson 1963; Levi 1969; Cramp 1986). (7) Male incubation: the duration (hours and minutes) of a male’s incubation period. We observed 21 males between days 0 and 19. Each pair was observed for a meanSE of 15.272.6 h (range 12–19 h). Female pigeons incubate the eggs overnight, swapping with males in the morning who are subsequently relieved by their partner about 2 h before dusk (Levi 1969). (8) Chick visit rate by males: pigeons feed chicks with crop milk for the first few days after hatching, after which seeds are mixed with milk (Vandeputte-Poma 1980). Crop milk has a high protein and lipid content and chicks are fed just three to four times each day (Davies 1939; Johnston 1992). As chick feeding could not be measured quantitatively, the number of times that a male entered the dovecote to attend to chicks was used as a measure of parental effort. We observed 21 males between days 18 and 30. Each pair was observed for a meanSE of 9.463.2 h (range 2–12 h).
Male Removal Experiments In 1994 and 1995, we performed a removal experiment to investigate the behaviour of fertile females in the absence of their male partner, and to determine whether mate guarding reduced the likelihood of a female being subjected to sexual harassment. In each of 10 trials, we observed for 1 h a pair in which the female was fertile. At the end of the hour we temporarily removed the male of the pair using a walk-in trap baited with food. We kept him in a cage measuring 503535 cm. In five trials, we left the cage in a position in which the captured male could be seen by his female, to prevent the female assuming she had been widowed. In the other five trials, the caged male was removed from the female’s sight. In all trials we recorded the behaviour of the female (as described above) in the absence of the male for 1 h before the male was released. Observations were then made for a further hour. A second experiment examined the ability of females to forage or feed in the presence and absence of their partner. During the hour prior to a removal, we offered a small amount (250 g) of mixed seed to the group of birds present at the site, and timed with a stopwatch the number of seconds that the focal female spent feeding in the following 3 min. We repeated this procedure during the hour when the female’s partner had been removed, and again during the hour after we released the male. Manipulations were carried out on pairs predicted to be fertile. After each experiment, we checked the nest of the manipulated pair every day until the first egg had been laid. Although the entire fertile period spans from day 10 to day 0 (Lovell-Mansbridge 1995), only pairs that had been caught between days 5 and 0 (10 pairs), and were therefore close to the peak of fertility, were included in the analysis. Means are expressedSE.
LOVELL-MANSBRIDGE & BIRKHEAD: COPULATION IN PIGEONS 237
0.8
Begs/h
0.6
0.4
0.2
0.0
Males
Females
1.0
(b) Proportion of copulations initiated
1.0
(a)
Proportion of begs leading to copulation
1.0
0.8
0.6
0.4
0.2
0.0
Males
Females
(c)
0.8
0.6
0.4
0.2
0.0
Males
Females
Figure 1. (a) Rate of begging (X+SE) by males and females during the fertile period (Mann–Whitney U test: males versus females: U=226, N1 =N2 =18, P<0.05). (b) Proportion of begs (X+SE by males and females that led to copulation (Mann–Whitney U test: males versus females: U=49.5, N1 =10, N2 =15, P=0.157). (c) Proportion of copulations initiated (X+SE; Mann–Whitney U test: males versus females: U=93, N1 =N2 =10, P=0.001).
RESULTS
Initiation of Copulation Of 337 copulations observed, the pair member initiating copulation was determined in 248 (73.6%) cases. Females initiated begging significantly more often than their partner (Fig. 1a); however, there was no difference between the proportion of male and female begs that led to a copulation (Fig. 1b). Overall, females initiated significantly more copulations than did males (Fig. 1c).
Copulation Rates and Intrapair Distance Between pairs, the mean copulation rate within pairs over the fertile period was significantly and negatively correlated with the mean intrapair distance (Fig. 2a). In addition, the rate at which females initiated pair copulations was significantly and negatively correlated with the intrapair distance for that pair (Fig. 2b). Moreover, the proportion of time that pairs spent within 10 m of each other also correlated significantly with the copulation rate (r13 =0.597, P<0.02). Thus those females that initiated more copulations from their partner received closer mate guarding. Changes in the distance between pairs could also be explained by the copulation access hypothesis, which states that the intrapair distance decreases as the male follows the female closely in order to be present when she solicits for copulation (Gowaty & Plissner 1987). However, there was no evidence for this since there was no difference between the intrapair distance in the 6 min before (0.670.2 m) and after (0.470.13 m) copulation (Wilcoxon signed-ranks test: T=29, N=17, P=0.433).
Removal Experiments There were no significant differences in the behaviour of females or extrapair males when removed pair males
were in sight or out of sight of their female, so the two sets of data were combined. In the absence of their partner, females were courted by other males for a significantly greater proportion of time (56.8%) than when their partner was present (3.7%; Fig. 3a). However, there was no difference in the frequency with which females approached other males (Fig. 3b) nor in the frequency of extrapair copulations (Wilcoxon signed-ranks test: T=0, N=10, P=0.317) when the female’s partner had been removed. When their partner was absent, females spent significantly less time feeding (0.680.18 min) than when he was present (1.580.313 min; Wilcoxon signed-ranks test: T=5, N=10, P=0.022). Females spent more time feeding (1.560.18 min) after the release of their partner than during the removal (Wilcoxon signed-ranks test: T=5, N=10, P=0.22).
Mate Guarding and Extrapair Behaviour During the fertile period males spent most of their time (90.3%) within 10 m of their female, and the mean distance between partners was 0.620.101 m; range 0–4.1 m). That this close proximity was related to the likelihood of harrassment by other males is demonstrated by the fact that other males approached the female more frequently as intrapair distance increased. The number of approaches per female per h increased from 1.370.21 to 3.020.44 to 3.760.34, over distances of 0–1, 1–2 and 2–3 m (Kruskal–Wallis: H2 =20.16, P=0.0001, N=16 pairs).
Copulation Rates and Parental Care by Males For 32 clutches from 21 pairs, all putative fathers took part in incubating eggs and young chicks, sitting for about 7 h during the day, from mid-morning (1040 hours15.5 min) until late afternoon (1730 hours 16.98 min). When chicks were old enough to be left unbrooded (day 9; Johnston 1992) males and females
238 ANIMAL BEHAVIOUR, 56, 1
Duration of courting (min) from extrapair males during pair
3
Pair copulations/h
(a)
2
1
50
40
30
20
10
0
1
2
3
3
Female initiation of copulation/h
(b)
2
1
Female approaches to extrapair males during hour
3 0
(a)
Absent
Present (b)
2
1
0
Absent
Present Pair male
0
1 2 Distance between mates (m)
3
Figure 2. Intrapair distance in relation to (a) copulation rate within pairs (Spearman rank correlation coefficient: rS = −0.724, N=16, P<0.01) and (b) the rate of female initiation of pair copulations (rS = −0.545, N=14, P<0.05). Each point represents the mean value from day −5 to day 0, for one pair of birds, where day 0 is the day the first egg was laid.
attended them with equal frequency (males: 4.830.55 times/h; females: 3.520.64 times/h; Mann– Whitney U test: U=99.5, N1 =N2 =12, P=0.109). Across pairs, the copulation rate during the fertile period was not correlated with either the duration of incubation by males (Spearman rank correlation coefficient: rS = 0.285, N=12, P=0.341) or the rate of chick attendance by males (Spearman rank correlation coefficient: rS = 0.309, N=12, P=0.318). DISCUSSION Many behaviours shown by socially monogamous male birds during the breeding season apparently function to prevent them from losing paternity of chicks that they
Figure 3. (a) Duration of courtship (X+SE) of fertile females by extrapair males in the presence and absence of the pair male (Wilcoxon signed-ranks test: presence versus absence: T=55, N=10, P<0.001). (b) Approaches by females (X+SE) to extrapair males in the presence and absence of the female’s mate (Wilcoxon signedranks test: presence versus absence: T=101, N=10, P=0.758).
help to rear (Birkhead & Møller 1992). The paternity assurance behaviours displayed by male pigeons are especially intense and include frequent copulations and mate guarding (Lovell-Mansbridge 1995). However, female pigeons initiated more pair copulations than their male partner. Furthermore, when freed from the constraints of intense mate guarding by the removal of their partner, females neither approached other males nor attempted to engage in extrapair copulations. Given these results, why do intense mate guarding by males and frequent copulation initiated mainly by females occur?
Benefits to Females of Frequent Copulations Several hypotheses account for repeated pair copulation from the female’s perspective; female pigeons might benefit in the following ways. (1) Females might have initiated frequent copulations with their partner to assure him of his paternity, as a male might invest more effort in rearing chicks if he is
LOVELL-MANSBRIDGE & BIRKHEAD: COPULATION IN PIGEONS 239
confident that they are his offspring (Burke et al. 1989). Parental investment by male pigeons is substantial. Males incubate the eggs throughout the day (Levi 1969) and both parents contribute equally to feeding the chicks (Vandeputte-Poma 1980; Westmoreland & Best 1987; Blockstein 1989). However, there was no correlation between copulation frequency within pairs and parental investment by males. (2) A female may use frequent copulation to reduce the likelihood that her partner copulates or forms a pair bond with another female (Petrie 1992). In the 3 years of this study, however, no males were polygynous, and the extrapair copulation rate was low (1.2% of copulations; Lovell-Mansbridge 1995), indicating that there would be little benefit to females of guarding their partners. Moreover, divorce and mate switching were also rare (Lovell-Mansbridge 1995). (3) Repeated pair copulations may also increase the chance that eggs will be fertilized (Birkhead et al. 1987; Adkins-Regan 1995; Lovell-Mansbridge 1995). However, both captive and wild pigeons have a low incidence of unhatched eggs (Murton & Clarke 1968; Levi 1969) and the number of spermatozoa recorded on the perivitelline layers of eggs exceeds that required for fertilization (Lovell-Mansbridge 1995). (4) Females may initiate frequent copulations to increase the amount of courtship feeding that they obtain from males (Hunter et al. 1993). In red-billed gulls, Larus novaehollandiae, copulation attempts were more successful when males fed females prior to mounting them (Tasker & Mills 1981). In this study, each of the 337 copulations observed was preceded by courtship feeding (billing), and on no other occasion were females seen to be fed by males. However, female pigeons did not appear to be dependent on the food delivered by males since, in this study at least, food was abundant. Furthermore, it appears that food is passed only rarely or in small amounts during billing (Cramp 1986). It is also unlikely that the diurnal increase in pair copulations found in pigeons (Lovell-Mansbridge 1995) could be explained by temporal changes in females’ requirements for food, as pigeons forage chiefly in the early morning and midafternoon (Johnston 1992). (5) A potential benefit of a male’s proximity to his mate is that the female is protected from the unwanted courtship of other males (Ashcroft 1976; Lumpkin 1983; Lamprecht 1989). In this study, courtship by other male pigeons was much more frequent during removal experiments than when the pair male was present, taking up 57% of the time and frequently resulting in aggression towards the female. As they were frequently interrupted by courting males, unguarded females spent less time feeding than guarded females. The time and energy lost by unguarded females while extrapair males court and harass them may represent a significant cost. Females may encourage the protection from harassment afforded by the close proximity of their mate, by initiating frequent copulations throughout their fertile period. Reduced harrassment of the female together with frequent pair copulation may also be beneficial to the male partner.
The fact that the copulation rate peaked in the fertile period is consistent with both the harassment hypothesis, and also with the sperm devaluation hypothesis and the fertilization hypothesis. Female manipulation of male protection may be more important during the fertile period than in the prefertile or postfertile periods as egg production may increase females’ energy demands (Walsberg 1983). Copulation frequency in pigeons increases during the day as well (Lovell-Mansbridge 1995) but it is unlikely that the benefit that females gain from male protection during feeding would also do so, so the harassment hypothesis cannot account for this diurnal increase.
Why do Female Pigeons not Seek Extrapair Copulations? Studies of other species that have involved the removal of male partners have sometimes resulted in increased extrapair copulation attempts by females, for example in barn swallows, Hirundo rustica (Møller 1987) and pied flycatchers, Ficedula hypoleuca (Bjo ¨ rklund & Westman 1983). In other species, however, females avoided extrapair copulation attempts, for example great tits, Parus major (Bjo ¨ rklund et al. 1992) and bar-headed geese (Lamprecht 1989). In pigeons, the close mate guarding of females by males and the high frequency of pair copulations suggests that the risk of extrapair copulation attempts was high. However, when pair males were removed females did not engage in extrapair copulations despite frequent courtship from other males. There are two possible reasons why females did not show any extrapair behaviour, the first being that the costs of extrapair copulations are high. Pair males may physically punish partners in response to cuckoldry: male ring doves behave aggressively towards females that have already copulated with other males, and breeding is delayed in females paired to aggressive males (Erickson & Zenone 1976; Zenone et al. 1979). In a species such as the pigeon, where pairs can produce six clutches per year (Murton et al. 1974; Johnston 1992) any delay in breeding could impose a cost in productivity. An alternative response of cuckolded males is the withdrawal of parental care (Trivers 1972). This could be extremely costly to female pigeons, as the dependence of chicks on crop milk produced by both parents means that biparental care is essential. A second explanation is that there may be no advantage to females in engaging in extrapair copulations. This is a difficult hypothesis to test since at present the benefits that females obtain from extrapair copulations in those species in which they occur are obscure (Birkhead, in press). In conclusion, our main finding was that female pigeons that initiated frequent copulations with their partners received significantly closer mate guarding from them. This close proximity was advantageous to females, since when mate guarding was prevented through the temporary removal of pair males, females suffered increased harassment from other males, which interfered with their ability to feed. Female pigeons may therefore use copulation solicitation to manipulate male proximity.
240 ANIMAL BEHAVIOUR, 56, 1
Acknowledgments We are extremely grateful to the Ramsden family for allowing us to work on their property and for their hospitality. B. J. Hatchwell, B. C. Sheldon and two anonymous referees made helpful comments on the manuscript. C. L.-M. was supported by a BBSRC studentship. References Adkins-Regan, E. 1995. Predictors of fertilization in the Japanese quail, Coturnix japonica. Animal Behaviour, 50, 1405–1415. Altmann, J. 1974. Observational study of behaviour: sampling methods. Behaviour, 49, 227–267. Ashcroft, R. E. 1976. A function of the pair bond in the common eider. Wildfowl, 27, 101–105. Birkhead, T. R. In press. Sperm competition in birds: mechanisms and function. In: Sperm Competition and Sexual Selection (Ed. by T. R. Birkhead & A. P. Møller), London: Academic Press. Birkhead, T. R. & Møller, A. P. 1992. Sperm Competition in Birds. Evolutionary Causes and Consequences. London: Academic Press. Birkhead, T. R., Atkin, L. & Møller, A. P. 1987. Copulation behaviour of birds. Behaviour, 101, 101–138. Birkhead, T. R., Pellatt, E. J. & Hunter, F. M. 1988. Extra-pair copulations and sperm competition in the zebra finch. Nature, 334, 60–62. Birkhead, T. M., Hunter, F. M. & Pellatt, E. J. 1989. Sperm competition in the zebra finch Taeniopygia guttata. Animal Behaviour, 38, 935–950. Birkhead, T. R., Wishart, G. J. & Biggins, J. D. 1995. Sperm precedence in domestic fowl. Proceedings of the Royal Society of London, Series B, 261, 255–292. Birkhead, T. R., Briskie, J. V., Lifjeld, J. T. & Slagsvold, T. 1997. Breeding-cycle patterns of sperm storage in the pied flycatcher (Ficedula hypoleuca). Auk, 114, 792–796. Bjo ¨ rklund, M. & Westman, B. 1983. Extra-pair copulations in the pied flycatcher (Ficedula hypoleuca). A removal experiment. Behavioral Ecology and Sociobiology, 13, 271–275. Bjo ¨ rklund, M., Møller, A. P., Sundberg, J. & Westman, B. 1992. Female great tits, Parus major avoid extra-pair copulation attempts. Animal Behaviour, 43, 691–693. Blockstein, D. E. 1989. Crop milk and clutch size in mourning doves. Wilson Bulletin, 101, 11–25. Burke, T., Davies, N. B., Bruford, M. W. & Hatchwell, B. J. 1989. Parental care and mating behaviour of polyandrous dunnocks Prunella modularis related to paternity by DNA fingerprinting. Nature, 338, 249–251. Colegrave, N., Birkhead, T. R. & Lessells, C. M. 1995. Sperm precedence in zebra finches does not require special mechanisms of sperm competition. Proceedings of the Royal Society of London, Series B, 259, 223–228. Cramp, S. (Ed.) 1986. Handbook of the Birds of Europe, the Middle East and North Africa. The Birds of the Western Palearctic. Vol. IV. Oxford: Oxford University Press. Davies, N. B., Hatchwell, B. J., Robson, T. & Burke, T. 1992. Paternity and parental effort in dunnocks, Prunella modularis: how good are chick-feeding rules? Animal Behaviour, 43, 729–745. Davies, W. L. 1939. The composition of the crop milk of pigeons. Journal of Biochemistry, 33, 898–901. Eens, M. & Pinxten, R. 1995. Inter-sexual conflicts over copulations in the European starling: evidence for the female mate-guarding hypothesis. Behavioural Ecology and Sociobiology, 36, 71–81. Enquist, M., Rosenberg, R. H. & Temrin, H. 1998. The logic of me´nage a` trois. Proceedings of the Royal Society of London, Series B, 265, 609–613.
Erickson, C. J. & Zenone, P. G. 1976. Courtship differences in male ring doves: avoidance of cuckoldry? Science, 192, 1353–1354. Fabricius, E. & Jansson, A. 1963. Laboratory observations on the reproductive behaviour of the ring dove during the pre-incubation phase of the breeding cycle. Animal Behaviour, 11, 534–539. Gowaty, P. A. & Plissner, J. H. 1987. Association of male and female American robins (Turdus migratorius) during the breeding season: paternity assurance by sexual access or mate-guarding? Wilson Bulletin, 199, 56–62. Heinroth, O. & Heinroth, K. 1949. Verhaltensweisen der Felsentaube (Haustaube) Columbia livia livia L. Zeitschrift fu¨r Tierpsychologie, 6, 153–201. Houston, A. I. 1995. Paternal effort and paternity. Animal Behaviour, 50, 1635–1644. Hunter, F. M., Petrie, M., Otronen, M., Birkhead, T. & Møller, A. P. 1993. Why do females copulate repeatedly with one male? Trends in Ecology and Evolution, 8, 21–26. Johnston, R. F. 1992. The rock dove. In: The Birds of North America (13) (Ed. by A. Poole, P. Stettenheim & F. Gill), pp. 1–16. Philadelphia: The Academy of Natural Sciences and Washington DC: The American Ornithologists’ Union. Kempenaers, B., Verheyen, G. R. & Dhondt, A. A. 1995. Mate-guarding and copulation behaviour in monogamous and polygynous blue tits: do males follow a best-of-a-bad-job strategy? Behavioral Ecology and Sociobiology, 36, 33–42. Lake, P. E. 1975. Gamete production and the fertile period with particular reference to domesticated birds. Symposia of the Zoological Society of London, 35, 225–244. Lamprecht, J. 1989. Mate-guarding in geese: awaiting female receptivity, protection of paternity or support of female feeding? In: The Sociobiology of Sexual and Reproductive Strategies (Ed. by C. A. E. Rasa, C. Vogel & E. Vogel), pp. 48–66. London: Chapman & Hall. Levi, W. 1969. The Pigeon. Sumter, South Carolina: Levi. Lovell-Mansbridge, C. 1995. Sperm competition in the feral pigeon Columba livia. Ph.D. thesis, University of Sheffield. Lumpkin, S. 1983. Female manipulation of male avoidance of cuckoldry behaviour in the ring dove. In: Behaviour of Female Vertebrates (Ed. by S. K. Wasser), pp. 91–112. London: Academic Press. Møller, A. P. 1987. Mate-guarding in the swallow Hirundo rustica: an experimental study. Behavioral Ecology and Sociobiology, 21, 119–123. Møller, A. P. & Birkhead, T. R. 1991. Frequent copulations and mate-guarding as alternative paternity guards in birds: a comparative study. Behaviour, 118, 170–186. Murton, R. K. & Clarke, S. P. 1968. Breeding biology of rock doves. British Birds, 61, 429–448. Murton, R. K., Thearle, R. J. P. & Coombs, C. F. B. 1974. Ecological studies of the feral pigeon Columba livia var. III Reproduction and plumage polymorphism. Journal of Applied Ecology, 11, 841– 854. Petrie, M. 1992. Copulation frequency in birds: why do females copulate more than once with the same male? Animal Behaviour, 44, 790–792. Sheldon, B. C. 1994. Male phenotype, fertility, and the pursuit of extra-pair copulations by female birds. Proceedings of the Royal Society of London, Series B, 257, 25–30. Tasker, C. R. & Mills, J. A. 1981. A functional analysis of courtship feeding in the red-billed gull Larus novaehollandiae scopulinus. Behaviour, 77, 222–241. Trivers, R. L. 1972. Parental investment and sexual selection. In Sexual Selection and the Descent of Man, 1871–1971 (Ed. by B. Campbell), pp. 136–179. Chicago: Aldine-Atherton. Vandeputte-Poma, J. 1980. Feeding, growth and metabolism of the pigeon, Columbia livia domesticus: duration and role of crop milk feeding. Journal of Comparative Physiology, 135, 97–99.
LOVELL-MANSBRIDGE & BIRKHEAD: COPULATION IN PIGEONS 241
Walsberg, G. E. 1983. Avian ecological energetics. In: Avian Biology (Ed. by D. S. Farner, J. R. King & K. C. Parkes), pp. 161–220. London: Academic Press. Westmoreland, B. & Best, L. B. 1987. What limits mourning doves to a clutch of two eggs? Condor, 89, 486–493.
Westneat, D. F. & Sherman, P. W. 1993. Parentage and the evolution of parental behaviour. Behavioral Ecology, 4, 66–77. Zenone, P. G., Sims, M. E. & Erickson, C. J. 1979. Male ring dove behaviour and the defense of genetic paternity. American Naturalist, 114, 615–626.
Do female pigeons trade pair copulations for protection? CLAIRE LOVELL-MANSBRIDGE & T. R. BIRKHEAD
Department of Animal and Plant Sciences, University of Sheffield (Received 1 August 1997; initial acceptance 16 September 1997; final acceptance 11 December 1997; MS. number: 5606)
ABSTRACT Male pigeons, Columba livia, employ intense mate guarding and frequent copulation apparently as strategies to ensure their paternity. The aim of this study was to investigate the benefits to females of mate guarding by males and frequent copulation. Field observations showed that females initiated the majority of copulations and females that solicited copulations more frequently were guarded more closely by their partner. Experimental removal of guarding male partners showed that: (1) unguarded, fertile females suffered increased harassment from extrapair males which reduced their foraging efficiency; and (2) unguarded, fertile females did not seek copulations with extrapair males. Various explanations for frequent pair copulation initiated by females are discussed and we conclude that female pigeons trade pair copulations for protection (mate guarding) against sexual harassment from other males.
In socially monogamous birds, the frequency with which pairs copulate prior to egg laying varies markedly across species (Birkhead et al. 1987). In a review of hypotheses proposed to explain this variation, Birkhead & Møller (1992) concluded that copulation frequency within pairs is best explained by the sperm devaluation hypothesis: copulations are more frequent in species where the risk of extrapair copulations is high because sperm from frequent pair copulations devalues the sperm of competing males. This is consistent with the known mechanism of sperm competition in birds (Birkhead et al. 1995; Colegrave et al. 1995). In many species, however, it is the female and not the male who initiates pair copulations (Birkhead & Møller 1992), so more recent studies have asked how females might benefit from repeated copulations with the same male (Petrie 1992; Hunter et al. 1993). Several hypotheses have been proposed to explain why females copulate at high frequency with their partner. (1) In species where parental care by males is important, females may encourage repeated copulations to assure their partner of his paternity. Males may be more likely to feed young if they have copulated with a female and thus are confident of their paternity (e.g. Burke et al. 1989; Davies et al. 1992; Westneat & Sherman 1993; Houston 1995). (2) Females may employ frequent copulation as a mate-guarding strategy, since males that copulate frequently with their partners may be less likely to mate with other females (Petrie 1992). For example, female starlings, Sturnus vulgaris, use copulation solicitations to
interrupt their males’ singing and thus prevent them from becoming polygynous (Eens & Pinxten 1995). (3) Multiple copulations may increase the likelihood of eggs being fertilized (Birkhead et al. 1987). However, as one or a few ejaculates usually contain enough sperm to fertilize all the eggs in a clutch (Birkhead et al. 1987), there is little evidence for this (Lake 1975; but see Adkins-Regan 1995). Frequent copulation is the primary paternity guard employed by many colonial breeding birds and birds of prey. In most other bird species, males guard their partner by close following during their fertile period (Birkhead et al. 1997). In many species frequent copulation and mate guarding appear to be alternatives (Møller & Birkhead 1991), but some species employ both paternity guards (e.g. Birkhead et al. 1988; Sheldon 1994). The benefits to males of guarding females have been demonstrated in studies where temporary removal of males has resulted in an increase in the number of extrapair copulations directed at their partner (e.g. Bjo ¨ rklund & Westman 1983; Møller 1987; Birkhead et al. 1989). However, observations on eider ducks, Somateria mollissima, ring doves, Streptopelia risoria, bar-headed geese, Anser indicus, and blue tits, Parus caeruleus, have shown that females may also benefit from mate guarding, as the close proximity of a pair male affords protection from the unwanted courtship of other males, and thus allows females to forage more efficiently (Ashcroft 1976; Lumpkin 1983; Lamprecht 1989; Kempenaers et al. 1995). Furthermore, Lumpkin (1983) suggested that female ring doves may actively manipulate mate guarding by males to extend the period over which they gain these benefits (see also Enquist et al. 1998).
Correspondence: T. R. Birkhead, Department of Animal and Plant Sciences, University of Sheffield, Sheffield S10 2TN, U.K. (email: [email protected]). 0003–3472/98/070235+07 $30.00/0
1998 The Association for the Study of Animal Behaviour
235
1998 The Association for the Study of Animal Behaviour
236 ANIMAL BEHAVIOUR, 56, 1
A previous study concluded that male feral pigeons, Columba livia, employ both frequent copulation and mate guarding as paternity guards (Lovell-Mansbridge 1995). Pigeons are colonial breeders and feed in flocks (Cramp 1986; Johnston 1992) and where they exist at high densities, aggressive competition for food and partners can occur (Murton et al. 1972; Johnston 1992). The high frequency of pair copulation and the intense mate guarding by males are consistent with sperm competition hypotheses as the temporal pattern of both behaviours closely matches the timing of the release of ova from the ovary (Lovell-Mansbridge 1995). However, as females of most bird species solicit copulations more often than males (Birkhead & Møller 1992), an explanation for the adaptive significance of frequent copulations for females is necessary. As pigeons forage and breed at high densities, and display intense paternity guards, we predicted that male removal experiments would increase the likelihood of extrapair copulation. Our aims in this study therefore were: (1) to determine why females initiate frequent copulations with their social partner; and (2) to determine how fertile female pigeons behave in the absence of their guarding partner.
METHODS Behavioural observations largely followed those in Lovell-Mansbridge (1995) but briefly were as follows. We observed 21 pairs of colour-ringed birds at a dovecote in Derbyshire, England, over three breeding seasons (1993–1995) from March until September, using focal group sampling (Altmann 1974). Each pair was observed for a meanSE of 22.733.8 h (range 4–50 h) between day 5 and day 0 (the day the first egg was laid). Observations began when the female of a pair was first located and lasted a minimum of 20 min for each pair; up to six pairs could be watched simultaneously. During each observation period, we recorded specific behaviours on a printed tick sheet. Behaviours relevant to this study were defined as follows. (1) Intrapair distance in metres, or if <1 m in centimetres. (2) Copulation initiation: the sequence of copulation begins when a bird begs for courtship feeding, by gentle pecking movements at the base of its partner’s bill (see also Fabricius & Jansson 1963). The female inserts her bill into that of the male, and he appears to regurgitate food; feeding is symbolic as food is rarely passed (Heinroth & Heinroth 1949). Courtship feeding is followed by copulation (Fabricius & Jansson 1963). The sex of the bird soliciting copulation by begging was recorded. (3) Copulation: the number of copulation attempts. (4) Moves followed: the number of moves of 10 m or more, initiated by a pair member, that were followed by the other pair member within 5 s. (5) Extrapair males: the number of other males within 10 m of the focal pair. (6) Duration of male courtship: male pigeons show a characteristic ‘bowing’ display towards females, in which
they ruffle their neck feathers and sweep their fanned tail along the ground whilst giving a display call (Fabricius & Jansson 1963; Levi 1969; Cramp 1986). (7) Male incubation: the duration (hours and minutes) of a male’s incubation period. We observed 21 males between days 0 and 19. Each pair was observed for a meanSE of 15.272.6 h (range 12–19 h). Female pigeons incubate the eggs overnight, swapping with males in the morning who are subsequently relieved by their partner about 2 h before dusk (Levi 1969). (8) Chick visit rate by males: pigeons feed chicks with crop milk for the first few days after hatching, after which seeds are mixed with milk (Vandeputte-Poma 1980). Crop milk has a high protein and lipid content and chicks are fed just three to four times each day (Davies 1939; Johnston 1992). As chick feeding could not be measured quantitatively, the number of times that a male entered the dovecote to attend to chicks was used as a measure of parental effort. We observed 21 males between days 18 and 30. Each pair was observed for a meanSE of 9.463.2 h (range 2–12 h).
Male Removal Experiments In 1994 and 1995, we performed a removal experiment to investigate the behaviour of fertile females in the absence of their male partner, and to determine whether mate guarding reduced the likelihood of a female being subjected to sexual harassment. In each of 10 trials, we observed for 1 h a pair in which the female was fertile. At the end of the hour we temporarily removed the male of the pair using a walk-in trap baited with food. We kept him in a cage measuring 503535 cm. In five trials, we left the cage in a position in which the captured male could be seen by his female, to prevent the female assuming she had been widowed. In the other five trials, the caged male was removed from the female’s sight. In all trials we recorded the behaviour of the female (as described above) in the absence of the male for 1 h before the male was released. Observations were then made for a further hour. A second experiment examined the ability of females to forage or feed in the presence and absence of their partner. During the hour prior to a removal, we offered a small amount (250 g) of mixed seed to the group of birds present at the site, and timed with a stopwatch the number of seconds that the focal female spent feeding in the following 3 min. We repeated this procedure during the hour when the female’s partner had been removed, and again during the hour after we released the male. Manipulations were carried out on pairs predicted to be fertile. After each experiment, we checked the nest of the manipulated pair every day until the first egg had been laid. Although the entire fertile period spans from day 10 to day 0 (Lovell-Mansbridge 1995), only pairs that had been caught between days 5 and 0 (10 pairs), and were therefore close to the peak of fertility, were included in the analysis. Means are expressedSE.
LOVELL-MANSBRIDGE & BIRKHEAD: COPULATION IN PIGEONS 237
0.8
Begs/h
0.6
0.4
0.2
0.0
Males
Females
1.0
(b) Proportion of copulations initiated
1.0
(a)
Proportion of begs leading to copulation
1.0
0.8
0.6
0.4
0.2
0.0
Males
Females
(c)
0.8
0.6
0.4
0.2
0.0
Males
Females
Figure 1. (a) Rate of begging (X+SE) by males and females during the fertile period (Mann–Whitney U test: males versus females: U=226, N1 =N2 =18, P<0.05). (b) Proportion of begs (X+SE by males and females that led to copulation (Mann–Whitney U test: males versus females: U=49.5, N1 =10, N2 =15, P=0.157). (c) Proportion of copulations initiated (X+SE; Mann–Whitney U test: males versus females: U=93, N1 =N2 =10, P=0.001).
RESULTS
Initiation of Copulation Of 337 copulations observed, the pair member initiating copulation was determined in 248 (73.6%) cases. Females initiated begging significantly more often than their partner (Fig. 1a); however, there was no difference between the proportion of male and female begs that led to a copulation (Fig. 1b). Overall, females initiated significantly more copulations than did males (Fig. 1c).
Copulation Rates and Intrapair Distance Between pairs, the mean copulation rate within pairs over the fertile period was significantly and negatively correlated with the mean intrapair distance (Fig. 2a). In addition, the rate at which females initiated pair copulations was significantly and negatively correlated with the intrapair distance for that pair (Fig. 2b). Moreover, the proportion of time that pairs spent within 10 m of each other also correlated significantly with the copulation rate (r13 =0.597, P<0.02). Thus those females that initiated more copulations from their partner received closer mate guarding. Changes in the distance between pairs could also be explained by the copulation access hypothesis, which states that the intrapair distance decreases as the male follows the female closely in order to be present when she solicits for copulation (Gowaty & Plissner 1987). However, there was no evidence for this since there was no difference between the intrapair distance in the 6 min before (0.670.2 m) and after (0.470.13 m) copulation (Wilcoxon signed-ranks test: T=29, N=17, P=0.433).
Removal Experiments There were no significant differences in the behaviour of females or extrapair males when removed pair males
were in sight or out of sight of their female, so the two sets of data were combined. In the absence of their partner, females were courted by other males for a significantly greater proportion of time (56.8%) than when their partner was present (3.7%; Fig. 3a). However, there was no difference in the frequency with which females approached other males (Fig. 3b) nor in the frequency of extrapair copulations (Wilcoxon signed-ranks test: T=0, N=10, P=0.317) when the female’s partner had been removed. When their partner was absent, females spent significantly less time feeding (0.680.18 min) than when he was present (1.580.313 min; Wilcoxon signed-ranks test: T=5, N=10, P=0.022). Females spent more time feeding (1.560.18 min) after the release of their partner than during the removal (Wilcoxon signed-ranks test: T=5, N=10, P=0.22).
Mate Guarding and Extrapair Behaviour During the fertile period males spent most of their time (90.3%) within 10 m of their female, and the mean distance between partners was 0.620.101 m; range 0–4.1 m). That this close proximity was related to the likelihood of harrassment by other males is demonstrated by the fact that other males approached the female more frequently as intrapair distance increased. The number of approaches per female per h increased from 1.370.21 to 3.020.44 to 3.760.34, over distances of 0–1, 1–2 and 2–3 m (Kruskal–Wallis: H2 =20.16, P=0.0001, N=16 pairs).
Copulation Rates and Parental Care by Males For 32 clutches from 21 pairs, all putative fathers took part in incubating eggs and young chicks, sitting for about 7 h during the day, from mid-morning (1040 hours15.5 min) until late afternoon (1730 hours 16.98 min). When chicks were old enough to be left unbrooded (day 9; Johnston 1992) males and females
238 ANIMAL BEHAVIOUR, 56, 1
Duration of courting (min) from extrapair males during pair
3
Pair copulations/h
(a)
2
1
50
40
30
20
10
0
1
2
3
3
Female initiation of copulation/h
(b)
2
1
Female approaches to extrapair males during hour
3 0
(a)
Absent
Present (b)
2
1
0
Absent
Present Pair male
0
1 2 Distance between mates (m)
3
Figure 2. Intrapair distance in relation to (a) copulation rate within pairs (Spearman rank correlation coefficient: rS = −0.724, N=16, P<0.01) and (b) the rate of female initiation of pair copulations (rS = −0.545, N=14, P<0.05). Each point represents the mean value from day −5 to day 0, for one pair of birds, where day 0 is the day the first egg was laid.
attended them with equal frequency (males: 4.830.55 times/h; females: 3.520.64 times/h; Mann– Whitney U test: U=99.5, N1 =N2 =12, P=0.109). Across pairs, the copulation rate during the fertile period was not correlated with either the duration of incubation by males (Spearman rank correlation coefficient: rS = 0.285, N=12, P=0.341) or the rate of chick attendance by males (Spearman rank correlation coefficient: rS = 0.309, N=12, P=0.318). DISCUSSION Many behaviours shown by socially monogamous male birds during the breeding season apparently function to prevent them from losing paternity of chicks that they
Figure 3. (a) Duration of courtship (X+SE) of fertile females by extrapair males in the presence and absence of the pair male (Wilcoxon signed-ranks test: presence versus absence: T=55, N=10, P<0.001). (b) Approaches by females (X+SE) to extrapair males in the presence and absence of the female’s mate (Wilcoxon signedranks test: presence versus absence: T=101, N=10, P=0.758).
help to rear (Birkhead & Møller 1992). The paternity assurance behaviours displayed by male pigeons are especially intense and include frequent copulations and mate guarding (Lovell-Mansbridge 1995). However, female pigeons initiated more pair copulations than their male partner. Furthermore, when freed from the constraints of intense mate guarding by the removal of their partner, females neither approached other males nor attempted to engage in extrapair copulations. Given these results, why do intense mate guarding by males and frequent copulation initiated mainly by females occur?
Benefits to Females of Frequent Copulations Several hypotheses account for repeated pair copulation from the female’s perspective; female pigeons might benefit in the following ways. (1) Females might have initiated frequent copulations with their partner to assure him of his paternity, as a male might invest more effort in rearing chicks if he is
LOVELL-MANSBRIDGE & BIRKHEAD: COPULATION IN PIGEONS 239
confident that they are his offspring (Burke et al. 1989). Parental investment by male pigeons is substantial. Males incubate the eggs throughout the day (Levi 1969) and both parents contribute equally to feeding the chicks (Vandeputte-Poma 1980; Westmoreland & Best 1987; Blockstein 1989). However, there was no correlation between copulation frequency within pairs and parental investment by males. (2) A female may use frequent copulation to reduce the likelihood that her partner copulates or forms a pair bond with another female (Petrie 1992). In the 3 years of this study, however, no males were polygynous, and the extrapair copulation rate was low (1.2% of copulations; Lovell-Mansbridge 1995), indicating that there would be little benefit to females of guarding their partners. Moreover, divorce and mate switching were also rare (Lovell-Mansbridge 1995). (3) Repeated pair copulations may also increase the chance that eggs will be fertilized (Birkhead et al. 1987; Adkins-Regan 1995; Lovell-Mansbridge 1995). However, both captive and wild pigeons have a low incidence of unhatched eggs (Murton & Clarke 1968; Levi 1969) and the number of spermatozoa recorded on the perivitelline layers of eggs exceeds that required for fertilization (Lovell-Mansbridge 1995). (4) Females may initiate frequent copulations to increase the amount of courtship feeding that they obtain from males (Hunter et al. 1993). In red-billed gulls, Larus novaehollandiae, copulation attempts were more successful when males fed females prior to mounting them (Tasker & Mills 1981). In this study, each of the 337 copulations observed was preceded by courtship feeding (billing), and on no other occasion were females seen to be fed by males. However, female pigeons did not appear to be dependent on the food delivered by males since, in this study at least, food was abundant. Furthermore, it appears that food is passed only rarely or in small amounts during billing (Cramp 1986). It is also unlikely that the diurnal increase in pair copulations found in pigeons (Lovell-Mansbridge 1995) could be explained by temporal changes in females’ requirements for food, as pigeons forage chiefly in the early morning and midafternoon (Johnston 1992). (5) A potential benefit of a male’s proximity to his mate is that the female is protected from the unwanted courtship of other males (Ashcroft 1976; Lumpkin 1983; Lamprecht 1989). In this study, courtship by other male pigeons was much more frequent during removal experiments than when the pair male was present, taking up 57% of the time and frequently resulting in aggression towards the female. As they were frequently interrupted by courting males, unguarded females spent less time feeding than guarded females. The time and energy lost by unguarded females while extrapair males court and harass them may represent a significant cost. Females may encourage the protection from harassment afforded by the close proximity of their mate, by initiating frequent copulations throughout their fertile period. Reduced harrassment of the female together with frequent pair copulation may also be beneficial to the male partner.
The fact that the copulation rate peaked in the fertile period is consistent with both the harassment hypothesis, and also with the sperm devaluation hypothesis and the fertilization hypothesis. Female manipulation of male protection may be more important during the fertile period than in the prefertile or postfertile periods as egg production may increase females’ energy demands (Walsberg 1983). Copulation frequency in pigeons increases during the day as well (Lovell-Mansbridge 1995) but it is unlikely that the benefit that females gain from male protection during feeding would also do so, so the harassment hypothesis cannot account for this diurnal increase.
Why do Female Pigeons not Seek Extrapair Copulations? Studies of other species that have involved the removal of male partners have sometimes resulted in increased extrapair copulation attempts by females, for example in barn swallows, Hirundo rustica (Møller 1987) and pied flycatchers, Ficedula hypoleuca (Bjo ¨ rklund & Westman 1983). In other species, however, females avoided extrapair copulation attempts, for example great tits, Parus major (Bjo ¨ rklund et al. 1992) and bar-headed geese (Lamprecht 1989). In pigeons, the close mate guarding of females by males and the high frequency of pair copulations suggests that the risk of extrapair copulation attempts was high. However, when pair males were removed females did not engage in extrapair copulations despite frequent courtship from other males. There are two possible reasons why females did not show any extrapair behaviour, the first being that the costs of extrapair copulations are high. Pair males may physically punish partners in response to cuckoldry: male ring doves behave aggressively towards females that have already copulated with other males, and breeding is delayed in females paired to aggressive males (Erickson & Zenone 1976; Zenone et al. 1979). In a species such as the pigeon, where pairs can produce six clutches per year (Murton et al. 1974; Johnston 1992) any delay in breeding could impose a cost in productivity. An alternative response of cuckolded males is the withdrawal of parental care (Trivers 1972). This could be extremely costly to female pigeons, as the dependence of chicks on crop milk produced by both parents means that biparental care is essential. A second explanation is that there may be no advantage to females in engaging in extrapair copulations. This is a difficult hypothesis to test since at present the benefits that females obtain from extrapair copulations in those species in which they occur are obscure (Birkhead, in press). In conclusion, our main finding was that female pigeons that initiated frequent copulations with their partners received significantly closer mate guarding from them. This close proximity was advantageous to females, since when mate guarding was prevented through the temporary removal of pair males, females suffered increased harassment from other males, which interfered with their ability to feed. Female pigeons may therefore use copulation solicitation to manipulate male proximity.
240 ANIMAL BEHAVIOUR, 56, 1
Acknowledgments We are extremely grateful to the Ramsden family for allowing us to work on their property and for their hospitality. B. J. Hatchwell, B. C. Sheldon and two anonymous referees made helpful comments on the manuscript. C. L.-M. was supported by a BBSRC studentship. References Adkins-Regan, E. 1995. Predictors of fertilization in the Japanese quail, Coturnix japonica. Animal Behaviour, 50, 1405–1415. Altmann, J. 1974. Observational study of behaviour: sampling methods. Behaviour, 49, 227–267. Ashcroft, R. E. 1976. A function of the pair bond in the common eider. Wildfowl, 27, 101–105. Birkhead, T. R. In press. Sperm competition in birds: mechanisms and function. In: Sperm Competition and Sexual Selection (Ed. by T. R. Birkhead & A. P. Møller), London: Academic Press. Birkhead, T. R. & Møller, A. P. 1992. Sperm Competition in Birds. Evolutionary Causes and Consequences. London: Academic Press. Birkhead, T. R., Atkin, L. & Møller, A. P. 1987. Copulation behaviour of birds. Behaviour, 101, 101–138. Birkhead, T. R., Pellatt, E. J. & Hunter, F. M. 1988. Extra-pair copulations and sperm competition in the zebra finch. Nature, 334, 60–62. Birkhead, T. M., Hunter, F. M. & Pellatt, E. J. 1989. Sperm competition in the zebra finch Taeniopygia guttata. Animal Behaviour, 38, 935–950. Birkhead, T. R., Wishart, G. J. & Biggins, J. D. 1995. Sperm precedence in domestic fowl. Proceedings of the Royal Society of London, Series B, 261, 255–292. Birkhead, T. R., Briskie, J. V., Lifjeld, J. T. & Slagsvold, T. 1997. Breeding-cycle patterns of sperm storage in the pied flycatcher (Ficedula hypoleuca). Auk, 114, 792–796. Bjo ¨ rklund, M. & Westman, B. 1983. Extra-pair copulations in the pied flycatcher (Ficedula hypoleuca). A removal experiment. Behavioral Ecology and Sociobiology, 13, 271–275. Bjo ¨ rklund, M., Møller, A. P., Sundberg, J. & Westman, B. 1992. Female great tits, Parus major avoid extra-pair copulation attempts. Animal Behaviour, 43, 691–693. Blockstein, D. E. 1989. Crop milk and clutch size in mourning doves. Wilson Bulletin, 101, 11–25. Burke, T., Davies, N. B., Bruford, M. W. & Hatchwell, B. J. 1989. Parental care and mating behaviour of polyandrous dunnocks Prunella modularis related to paternity by DNA fingerprinting. Nature, 338, 249–251. Colegrave, N., Birkhead, T. R. & Lessells, C. M. 1995. Sperm precedence in zebra finches does not require special mechanisms of sperm competition. Proceedings of the Royal Society of London, Series B, 259, 223–228. Cramp, S. (Ed.) 1986. Handbook of the Birds of Europe, the Middle East and North Africa. The Birds of the Western Palearctic. Vol. IV. Oxford: Oxford University Press. Davies, N. B., Hatchwell, B. J., Robson, T. & Burke, T. 1992. Paternity and parental effort in dunnocks, Prunella modularis: how good are chick-feeding rules? Animal Behaviour, 43, 729–745. Davies, W. L. 1939. The composition of the crop milk of pigeons. Journal of Biochemistry, 33, 898–901. Eens, M. & Pinxten, R. 1995. Inter-sexual conflicts over copulations in the European starling: evidence for the female mate-guarding hypothesis. Behavioural Ecology and Sociobiology, 36, 71–81. Enquist, M., Rosenberg, R. H. & Temrin, H. 1998. The logic of me´nage a` trois. Proceedings of the Royal Society of London, Series B, 265, 609–613.
Erickson, C. J. & Zenone, P. G. 1976. Courtship differences in male ring doves: avoidance of cuckoldry? Science, 192, 1353–1354. Fabricius, E. & Jansson, A. 1963. Laboratory observations on the reproductive behaviour of the ring dove during the pre-incubation phase of the breeding cycle. Animal Behaviour, 11, 534–539. Gowaty, P. A. & Plissner, J. H. 1987. Association of male and female American robins (Turdus migratorius) during the breeding season: paternity assurance by sexual access or mate-guarding? Wilson Bulletin, 199, 56–62. Heinroth, O. & Heinroth, K. 1949. Verhaltensweisen der Felsentaube (Haustaube) Columbia livia livia L. Zeitschrift fu¨r Tierpsychologie, 6, 153–201. Houston, A. I. 1995. Paternal effort and paternity. Animal Behaviour, 50, 1635–1644. Hunter, F. M., Petrie, M., Otronen, M., Birkhead, T. & Møller, A. P. 1993. Why do females copulate repeatedly with one male? Trends in Ecology and Evolution, 8, 21–26. Johnston, R. F. 1992. The rock dove. In: The Birds of North America (13) (Ed. by A. Poole, P. Stettenheim & F. Gill), pp. 1–16. Philadelphia: The Academy of Natural Sciences and Washington DC: The American Ornithologists’ Union. Kempenaers, B., Verheyen, G. R. & Dhondt, A. A. 1995. Mate-guarding and copulation behaviour in monogamous and polygynous blue tits: do males follow a best-of-a-bad-job strategy? Behavioral Ecology and Sociobiology, 36, 33–42. Lake, P. E. 1975. Gamete production and the fertile period with particular reference to domesticated birds. Symposia of the Zoological Society of London, 35, 225–244. Lamprecht, J. 1989. Mate-guarding in geese: awaiting female receptivity, protection of paternity or support of female feeding? In: The Sociobiology of Sexual and Reproductive Strategies (Ed. by C. A. E. Rasa, C. Vogel & E. Vogel), pp. 48–66. London: Chapman & Hall. Levi, W. 1969. The Pigeon. Sumter, South Carolina: Levi. Lovell-Mansbridge, C. 1995. Sperm competition in the feral pigeon Columba livia. Ph.D. thesis, University of Sheffield. Lumpkin, S. 1983. Female manipulation of male avoidance of cuckoldry behaviour in the ring dove. In: Behaviour of Female Vertebrates (Ed. by S. K. Wasser), pp. 91–112. London: Academic Press. Møller, A. P. 1987. Mate-guarding in the swallow Hirundo rustica: an experimental study. Behavioral Ecology and Sociobiology, 21, 119–123. Møller, A. P. & Birkhead, T. R. 1991. Frequent copulations and mate-guarding as alternative paternity guards in birds: a comparative study. Behaviour, 118, 170–186. Murton, R. K. & Clarke, S. P. 1968. Breeding biology of rock doves. British Birds, 61, 429–448. Murton, R. K., Thearle, R. J. P. & Coombs, C. F. B. 1974. Ecological studies of the feral pigeon Columba livia var. III Reproduction and plumage polymorphism. Journal of Applied Ecology, 11, 841– 854. Petrie, M. 1992. Copulation frequency in birds: why do females copulate more than once with the same male? Animal Behaviour, 44, 790–792. Sheldon, B. C. 1994. Male phenotype, fertility, and the pursuit of extra-pair copulations by female birds. Proceedings of the Royal Society of London, Series B, 257, 25–30. Tasker, C. R. & Mills, J. A. 1981. A functional analysis of courtship feeding in the red-billed gull Larus novaehollandiae scopulinus. Behaviour, 77, 222–241. Trivers, R. L. 1972. Parental investment and sexual selection. In Sexual Selection and the Descent of Man, 1871–1971 (Ed. by B. Campbell), pp. 136–179. Chicago: Aldine-Atherton. Vandeputte-Poma, J. 1980. Feeding, growth and metabolism of the pigeon, Columbia livia domesticus: duration and role of crop milk feeding. Journal of Comparative Physiology, 135, 97–99.
LOVELL-MANSBRIDGE & BIRKHEAD: COPULATION IN PIGEONS 241
Walsberg, G. E. 1983. Avian ecological energetics. In: Avian Biology (Ed. by D. S. Farner, J. R. King & K. C. Parkes), pp. 161–220. London: Academic Press. Westmoreland, B. & Best, L. B. 1987. What limits mourning doves to a clutch of two eggs? Condor, 89, 486–493.
Westneat, D. F. & Sherman, P. W. 1993. Parentage and the evolution of parental behaviour. Behavioral Ecology, 4, 66–77. Zenone, P. G., Sims, M. E. & Erickson, C. J. 1979. Male ring dove behaviour and the defense of genetic paternity. American Naturalist, 114, 615–626.