The effect of breeding density and male quality on paternity-assurance behaviours in the house sparrow, Passer domesticus

Transcription

1 DOI /s ARTICLE The effect of breeding density and male quality on paternity-assurance behaviours in the house sparrow, Passer domesticus Herbert Hoi Hans Tost Matteo Griggio Received: 8 January 2009 / Accepted: 14 April 2010 Ó Japan Ethological Society and Springer 2010 Abstract Several factors can influence the risk of cuckoldry through extra-pair paternity for male birds. The number of neighbouring males is thought to affect the chance of females engaging in extra-pair copulations, and species which breed both socially (colonially) and solitarily provide an ideal opportunity to test the effect of close proximity on extra-pair behaviour and paternity guards. In this study, the extent to which male house sparrows, Passer domesticus, used two alternative strategies, namely frequent copulation and mate-guarding, to ensure paternity was investigated. We also examined how males vary the two paternity guards according to their breeding sociality. Pairs at the dense colony started to copulate at a higher rate at the beginning of the fertile period than those of the medium-sized colony and solitary breeding pairs. Male house sparrows appear to fine-tune their strategies according to the breeding density. Both strategies are alternatively used in the weak fertile period but are simultaneously used in the peak fertile period. Our results suggest that males modify their strategy according to their individual abilities: mate-guarding intensity was positively correlated with the black breast badge size. Keywords Badge of status Coloniality Extra-pair paternity Paternity guards Sexual selection Social behaviour H. Hoi H. Tost M. Griggio (&) Konrad Lorenz Institute for Ethology, Savoyenstrasse 1 a, 1160 Vienna, Austria m.griggio@klivv.oeaw.ac.at Introduction Many studies have demonstrated that extra-pair copulations are a strategy adopted by males to increase their reproductive success while females may obtain genetic benefits. Indeed, multiple mating can increase offspring performance and sexual attractiveness of sons (Jennions and Petrie 2000; Griffith et al. 2002; Westneat and Stewart 2003; Akçay and Roughgarden 2007). Male behavioural adaptations which evolve through sperm competition are strategies to ensure paternity. The two main mechanisms are mate-guarding behaviour and frequent copulations (Birkhead and Møller 1992a). Both mateguarding and frequent copulations are regarded as alternative compensatory paternity guards in the sense that, in general, the presence of one means the lack of the other and vice versa (Møller and Birkhead 1991). As mate-guarding is very timeconsuming (Pilastro et al. 2002), frequent copulations seem to be a logical alternative, for instance, in colonial seabirds (Birkhead 1978), where one partner has to stay near the nest site to defend the nest during the feeding trips of the other. With many neighbouring males, fertile females cannot be guarded properly and several authors have suggested that the risk of cuckoldry increases with colony size and density (Gladstone 1979; Møller 1985, 1987a; Wittenberger and Hunt 1985). For example, in raptors, the sperm competition intensity increases with breeding density, and males rely on frequent copulations to ensure paternity (Mougeot 2004). Unless copulations are very costly for the male, however, there is no reason why males of mate-guarding species should not also copulate frequently to increase paternity certainty. For example, Sheldon (1994) showed that male chaffinches, Fringilla coelebs, perform both strategies; males guard and at the same time they frequently copulate with their females.

2 In semicolonial species, where males very often experience varying breeding densities, one would expect that they should be able to change the strategy according to the social situation (e.g. number of neighbouring males; for a review, see Møller and Birkhead 1993). Males may also benefit from being able to modify their strategy throughout the female fertile period and according to the number of intrusions by other males (Møller 1985; Pinxten et al. 1987). Owing to last-male sperm precedence (Birkhead and Møller 1992b), one would predict that copulations immediately prior to fertilisation (in birds: 24 h prior to egglaying) would be the most successful (Birkhead et al. 1988, 1995; Colegrave et al. 1995), and, therefore, copulation frequency should peak just before and during egg-laying. Males may also modify their strategy according to their abilities. For instance, high-quality males might be able to guard the female efficiently while maintaining other behaviours like nest-guarding, territorial defence or frequent copulations at the same time. The aim of this study on house sparrows, Passer domesticus, was to investigate: (1) which paternity guard males adopt in relation to their degree of breeding sociality; (2) whether the two paternity guards are alternative strategies; (3) the timing of paternity guards during the female fertile cycle; and (4) their relation to male quality. The socially monogamous house sparrow is ideal for this type of study since: (1) it nests both solitarily as well as in dense colonies (Summers-Smith 1954); (2) it is known from other studies that it is subject to sperm competition (Wetton and Parkin 1991), and that about 27% of the nests contain extra-pair offspring and 14% of the offspring originate from extra-pair copulations (Wetton and Parkin 1991); and (3) the black breast badge of the male seems to play a role in female mate choice (Møller 1987b), although several studies failed to find such female preference (see Study species ). Moreover, males with larger badges engage in extra-pair copulation attempts more frequently than those with smaller badges, and it seems that males with larger badges are more efficient mate-guarders than small-badged males (Møller 1987c). Materials and methods Study species The house sparrow is an important model organism in evolutionary biology and behavioural ecology for the study of sexual selection in relation to plumage variation (e.g. Møller 1987b; Veiga and Puerta 1996; Moreno-Rueda 2005; for a review, see Nakagawa et al. 2007). The black throat patch of the male house sparrow seems to be an honest indicator of condition (Møller 1987b; Veiga and Puerta 1996; but see Nakagawa et al. 2007). It is often referred to as a badge of status (it is a predictor of dominance rank), and seems to be involved in female mate choice, but there are differences between populations (for a review, see Nakagawa et al. 2007). In a Danish population, males with large badges obtained a mate earlier during the breeding season than males with small badges. Females displayed more copulation solicitations in front of male dummies with large badges. Moreover, large-badged males were cuckolded less than small-badged males (Møller 1990). On the other hand, on Lundy Island, 20 km off the south-west coast of Britain, females preferred males with smaller badges and produced higher numbers of offspring with such males (Griffith et al. 1999). In an Austrian population, paternity losses were related to badge size. In particular, males with the smallest and largest badges were cuckolded less than those with average badges (Václav et al. 2002), even if the time mates spent together at the nest was positively correlated with badge size. Lastly, paternity assurance behaviours did not seem to be related to colony size in that population (Václav and Hoi 2002). Fieldwork The study was conducted in Soest, Germany ( N, E) during a single breeding season, The study included a medium-sized (20 25 breeding pairs) and a large house sparrow colony (including about 250 breeding pairs) on two similar sized farms, respectively, and 10 solitary breeding pairs in a nearby settlement. The three colony types were at least 10 km apart with open fields inhabited by breeding kestrels (Falco tinnunculus) in between, which represents a natural barrier for house sparrows to cross. The ten solitary pairs have been found on single family houses in a settlement, each nest at least 200 m apart. The large colony had pairs nesting in more than one farm building, and there was little interaction between those pairs or aggregations of pairs nesting at locally separated breeding sites within the farm (unpublished results). We therefore further separated the large colony into smaller subsets with a varying number of breeding pairs nesting at the same location, e.g. the same wall on a building. Thus, the breeding density at the large colony varied from solitary pairs to aggregations of up to seven pairs per site. Birds were mist-netted and individually colour-ringed prior to egg-laying. Nest-building started in the first week of April and dates of the first egg ranged from 13 April to 2 July. Modal clutch size was three eggs (range 2 7). Behavioural data were collected from solitary pairs, focal pairs of a medium-sized (consisting of 20 breeding pairs) and focal pairs of a large colony (consisting of around 250 breeding pairs). Observations were restricted to

3 about a distance of 50 m around the nest site. Copulations occur near or at the nest (Václav and Hoi 2002; own unpublished results). Each pair was observed for three successive breeding attempts. Daily investigations on behaviour started days prior to the start of egg-laying and ended 5 days after the start of incubation. Pairs of each colony were observed with a telescope for 15 min; every 10 s, behaviours of males and females were recorded, from a distance of about 20 m. Colonies were watched early in the morning in a rotating schedule to avoid individual nests being investigated at the same time each day. During the 15-min observation period, copulations, male and female arrivals near (within 10 m) or at the nest and departure times were recorded in order to calculate (1) the nest attendance for both pair members (min/15 min), (2) the period a pair spent together near or at the nest (min/15 min), and (3) to what extent males followed their females away from the nest (proportion). Following was defined as departure by the female in the course of which the male followed within a period of 10 s. In order to investigate the male s timing of paternity guards (min/15 min), male copulation behaviour (no. copulation/15 min) and male mate-guarding behaviour [i.e. time a pair spent together at the nest (min/15 min), percentage of trips in which a male followed the female] were recorded during the female fertile period, here defined as from day -9 to the day the penultimate egg was laid (where day 0 is the day when the first egg was laid). The fertile period was divided into a weak fertile period assuming a lower fertilisation probability, that is day -9 to day -2, and a peak fertile period assuming a higher fertilisation probability, from day -1 until the day when the penultimate egg was laid (see also Birkhead and Møller 1992a). In house sparrows, copulations are usually not evenly distributed over the time of the day but very often occur in bouts. Such copulation bouts consist of 2 9 copulations in rapid succession (usually only few seconds apart) (see Birkhead and Møller 1992a). Copulation frequency per bout also varies throughout the female fertile cycle with most bouts occurring during peak fertility. We used every copulation with cloacal contact to calculate copulation frequency. To determine which paternity guard was used under different social situations we divided the analyses into two parts. The frequency and timing of paternity assurance behaviour were compared, firstly, across colonies with a viewpoint from colony size (solitary, medium-sized and large colony). For this, we used ten solitary pairs, ten randomly selected focal pairs from the medium-sized and from a large colony, respectively. Secondly, we analysed correlations between paternity assurance behaviour and density. In this case, we used breeding density as the number of nests found on the same building substrate (e.g. one wall of a building) within the large colony. These building substrates are visually and locally separated and constitute breeding sites (units) with a varying number of breeding pairs including 1 7 pairs/site. In total, 17 visually- and locally-separated breeding sites were considered (10 breeding sites with one nest, 2 breeding sites with three nests, 2 breeding sites with four nests, 1 breeding site with five nests, 2 breeding sites with seven nests). All pairs of each breeding density were investigated. Thus, the total sample size is 43 breeding pairs. To determine whether paternity guards (e.g. intensity of mate-guarding and copulation frequency) were related to male quality, different morphological measurements including dimension of breast patches (badge size = 166.7? badge length 9 badge width; Møller 1987b), wing and tarsus length (to the nearest 0.1 mm) and body weight (to the nearest 0.1 g) were taken (Svensson 1992) from 36 males of the dense colony, 10 males from the medium-sized colony and 7 solitary breeding males. Statistical analyses Since behavioural parameters, in particular copulation behaviour, were in a far from linear and normal distribution (Birkhead and Møller 1992a), we used non-parametric analyses of variance to compare copulation and mateguarding frequency across the three colony sizes (pairs breeding solitarily, in a medium sized colony and in a large colony). We found no significant difference in the average copulation frequency between the three successive breeding attempts of each pair for none of the three colony sizes (Friedman test, for all P [ 0.2) and we also did not find any difference in average male-following behaviour (Friedman test, P [ 0.3). Therefore, we combined the three broods of each pair into one mean for each pair and ran a Kruskal Wallis test to compare the nesting situations. To test which groups specifically differ from each other, we used Dunn s multiple pairwise comparisons. To detect at which time during the breeding period the importance of colony size is most pronounced, we used a Kruskal Wallis test to compare copulation and mate-guarding frequency between the three colony sizes on a daily bases. Throughout, we used average copulation frequency, average time pair spent together at the nest and average male-following behaviour per breeding pair or colony size, and we used Spearman rank correlations to investigate the relationship between paternity guards and breeding density. To examine the relationship between male morphology and colony size, we firstly compared the three colony types (large and medium-sized colony and solitary breeding pairs) and secondly correlated the local breeding density with male

4 morphological traits. Means of morphological parameters for each breeding site were used. To examine the relationship between male paternity guards and male morphology, a partial correlation was used whereby we controlled for the effect of breeding density. For statistical analyses, we used the statistical package of SPSS (Norušis 1993). Results Copulation behaviour Copulations started on day -9, and copulation frequency peaked around day 0 and remained at a very high level until the day when the penultimate egg was laid (Fig. 1a). All copulations occurred during the early morning ( hours) and were solicited by the female. On average, each pair copulated 320 ± 6.3 (SE) times during the female fertile period based on the 20 focal pairs of the medium-sized and large colony. Copulation frequency significantly differed between colony sizes (Kruskal Wallis test, T = 16.03, df = 2, P \ ). Post hoc pairwise comparisons revealed that this difference is mainly due the significantly higher copulation frequency found in the large colony over the solitary and medium-sized colony situation (P \ 0.05) whereas the copulation frequency did not significantly differ between pairs in a medium-sized colony or solitary breeding pairs (P [ 0.2). A daily comparison showed significant differences between the three colony sizes for day -7 to day -4 (Kruskal Wallis test, for all P \ 0.05). Pairs in the large colony started to copulate at a higher rate at the beginning of the fertile period than those in the medium-sized colony and solitary breeding pairs (Fig. 1a). Splitting the large colony into smaller, locallyisolated subsets of breeding pairs also revealed a positive correlation between copulation frequency and the number of breeding pairs/site during the peak fertile period (r = 0.89, P \ 0.001, n = 17; Fig. 2a), but no relationship a b c Copulations / 15 min % male following Pair together / 15 min Days in relation to start of egg laying Fig. 1 a Mean copulation frequency of house sparrows, Passer domesticus, b the percentage the male follows the female when she leaves the nest, and c the time (in %) a pair spent together at or near the nest (within a 10 m radius), 15 min for ten pairs in each situation, in relation to the start of egg-laying (where day 0 is the day when the first egg was laid) for the large colony (circles), the medium-sized colony (triangles) and solitary breeding pairs (squares). Since there is no difference in the copulation pattern for three successive breeding attempts for all colony sizes (see text), data were pooled a b c Copulations / 15 min 4,0 3,5 3,0 2,5 2,0 1,5 1,0 0, Male following (%) / 15 min Time pair together /15 min Breeding pairs Breeding pairs Breeding pairs Fig. 2 Relationship between number of breeding pairs/breeding site within the dense colony and a copulation frequency, b the percentage the male follows the female when she leaves the nest, and c time a pair spent together (min) for 15 min in the weak (day -9 to day -2, circles) and the peak fertile periods (day -1 to the day when the penultimate egg was laid, squares). Data for the three breeding attempts were pooled

5 existed during the weak fertile period (r =-0.05, P [ 0.8, n = 17). We obtained the same result when we examined each breeding attempt separately (Table 1). Mate-guarding behaviour Male-following behaviour increased rapidly around day-7, remained high until the first egg was laid (Fig. 1b) and ceased completely after clutch completion. Male-following behaviour significantly differed between the three colony sizes (Kruskal Wallis test, T = 19.6, df = 2, P \ ). Post hoc pairwise comparisons revealed that this difference is mainly due to the significantly reduced male-following behaviour in the large over the solitary and medium-sized colony situation (P \ 0.05) whereas male-following frequency did not significantly differ between pairs in a medium-sized colony and solitary breeding pairs (P [ 0.2). The daily comparison between the three colony situations revealed differences only for days -7, -6 and-4(kruskal Wallis test, T = 12.1, df = 2, P \ 0.05). This means that, in the large colony, mate-guarding was less frequent during the weak fertile period but was relatively high during the peak fertile period (Fig. 1b). There was no significant correlation between male-following behaviour and the number of breeding pairs/ breeding site in either the weak (r =-0.25, P [ 0.3, n = 17) or the peak fertile period (r =-0.23, P [ 0.3, n = 17) (Fig. 2b). Examination of the three broods separately (see Table 1) showed a significant negative correlation between mate-guarding and breeding density only during the weak fertile period of the third breeding attempt. During the peak fertile period, following behaviour did not appear to be influenced by breeding density (Table 1). The amount of time a pair spent together at or near the nest increased from day -9, peaked at day -1 and then decreased again at the start of egg-laying (Fig. 1c). The time spent together differed significantly with breeding density (Friedman test, T = 7.7, df = 15, P = 0.02). Daily comparisons showed significant differences nearly every day (Kruskal Wallis tests, df = 2, for all days P \ 0.05, except day?4 P [ 0.1). The time spent together at or near the nest in the large colony was lowest prior to egg-laying and highest during egg-laying (Fig. 1c). The time a pair spent together was negatively correlated with breeding density in the weak fertile period (r = -0.70, P \ 0.002, n = 17) but positively correlated with breeding density during the peak fertile period (r = 0.59, P \ 0.01, n = 17) (Fig. 2c). The negative correlation in the weak fertile period occurred in all breeding attempts (Table 1) but the positive correlation during the peak fertile period was significant only for the first brood (Table 1). These differences are not because of differences in female behaviour, since nest-attendance of females did not vary in relation to colony size (Kruskal Wallis test, for the weak fertile period: T = 2.59, df = 2, P [ 0.2; for the peak fertile period: T = 1.9, df = 2, P [ 0.3) and did not depend on breeding density (Kruskal Wallis test, for the weak fertile period: T = 7.9, df = 7, P [ 0.3; for the peak fertile period: T = 6.6, df = 7, P [ 0.4). There is not even a tendency of female nest-attendance in any direction (weak fertile period: r = 0.07, P [ 0.8, n = 17; peak fertile period: r = 0.03, P [ 0.9, n = 17). Comparison of the two paternity guards (Fig. 1) suggests that they are used alternatively in the weak fertile period, since copulation frequency is higher and guarding behaviour is lower in pairs of dense colonies. No such inverse relationship could, however, be detected during the peak fertile period. Correlation of the two paternity guards (frequent copulations with male-following behaviour and the time a pair spent together) of individual males revealed no relation during the weak fertile period (with following behaviour: r = 0.14, P [ 0.4, n = 30; with the time a pair spent together: r =-0.3, P [ 0.1, n = 30) but a positive correlation with both mate-guarding parameters during the peak fertile period (with following behaviour: r = 0.52, P \ 0.004, n = 30; with the time a pair spent together: r = 0.49, P \ 0.007, n = 30). Examination of the relationship between the two mateguarding parameters showed that they are positively correlated during the weak fertile period (r = 0.49, P = 0.006) but they seem to be independent during peak fertility (r = 0.22, P [ 0.2). Table 1 Correlation coefficients (r) and significance values (P) between copulation frequency, percentage of times male house sparrows, Passer domesticus, followed the female and the time a pair spent together with nest density/breeding site for the weak and the peak fertile periods for all three breeding attempts Copulation frequency Male following female Time together Weak Peak Weak Peak Weak Peak First brood 0.20 [ < [ [ < <0.003 Second brood 0.05 [ < [ [ < [0.2 Third brood [ < < [ < [0.2 Statistically significant values are in bold. n = 17 for all

6 Morphology and paternity guards Breast patches are biggest in males of the large colony and smallest in solitary breeding males. Tarsus length is smallest in males of the medium-sized colony (Table 2). Average breast-patch size/site also increased with increasing local breeding density within the large breeding colony (r = 0.50, P \ 0.03, n = 17). Average weight/site (r =-0.45, P [ 0.05, n = 17) and average tarsus length/ site (r =-0.43, P [ 0.06, n = 17) tended to decrease with local density, whereas average wing length/site was not related to varying breeding density (r =-0.05, P [ 0.8, n = 17). The body weight, wing and tarsus length were not significantly correlated with paternity-guard behaviours (all P [ 0.3). On the contrary, males with bigger patches achieved higher copulation frequencies and spent more time together with their females during the peak fertile period (r = 0.51, P = 0.02; r = 0.48, P = 0.03, respectively). During the weak fertile period, patch size was negatively related to the time a pair spent together (r =-0.48, P = 0.04). Controlling for the possible effects of breeding sociality (density) a partial correlation revealed that only one mateguarding factor, time together, was significantly related to patch size during peak fertility (r part = 0.47, P = 0.04, n = 19) but there was no relation between patch size and copulation frequency during the peak fertile period (r part = 0.39, P = 0.1, n = 19) nor during time spent together during the weak fertile period (r part =-0.15, P [ 0.5, n = 19). Discussion Do males really use both paternity guards? Since house sparrows copulate about 300 times per breeding cycle, they can be claimed as a frequently-copulating species like dunnocks Prunella modularis (Hatchwell and Davies Table 2 Different morphological features (± SE) of males of the large (n = 36 males) and the medium-sized colony (n = 10 males) and of solitary breeding pairs (n = 7 males) Large Medium Solitary P Weight (g) 31.7 (0.3) 30.6 (0.4) 30.7 (1.5) [0.3 Wing length (mm) 73.6 (0.9) 73.5 (2.2) 70.3 (1.0) [0.4 Tarsus length (mm) 19.6 (0.2) 18.7 (0.3) 20.2 (0.9) [0.05 Patch size (mm 2 ) (7.1) (12.8) (22.7) <0.05 The significance values (P) are revealed by a comparison of the three colony situations according to a Kruskal Wallis test. Statistically significant values are in bold 1992), chaffinches (Sheldon 1994) or Smith longspurs Calcarius pictus (Briskie 1990). The way in which the intensity of mate-guarding in sparrows varies with regard to the female cycle is similar to that of other territorial passerines (e.g. Kempenaers et al. 1992). At the peak of mateguardingn male house sparrows follow their females on almost 90% of occasions, which is comparable to the behaviour of other mate-guarding species like magpies Pica pica with 95% (Birkhead 1982), starlings Sturnus vulgaris with 100% (Pinxten et al. 1987) or American robins Turdus migratorius (Gowaty and Plissner 1987). If the behaviours identified as paternity guards (mateguarding and frequent copulation) are indeed behavioural adaptations to guard paternity, then their variation from day-to-day over the female cycle should be related to the risk of losing paternity on that day. The risk that an extrapair copulation leads to an extra-pair fertilisation increases as egg-laying approaches. This has partly to do with the mechanism of sperm precedence (Birkhead et al. 1988, 1995; Colegrave et al. 1995). In addition, because males are likely to have an increasing amount of information about when their female is going to lay as egg-laying approaches, the expected value of a female as a resource increases through the female fertile period, and male investment should therefore be in proportion to the expected reward on each day of the female cycle (Dawkins and Carlisle 1976). Several of our observations suggest that male paternity guards do vary with female fertility as predicted. Male mateguarding intensity, measured as the time a pair spent together and the proportion of female moves from the nest that are followed by the male, varied within the cycle and peaked around day -1 to day 0. Copulation frequency also increased during the fertile period and peaked around day 0. Like many other colonial birds, male sparrows are faced with the trade-off between defending the nest site and guarding the mate. This trade-off may, however, be less pronounced when copulations extra-pair as well as withinpair occur only at the nest as with the house martin Delichon urbica (Lifjeld and Marstein 1994). In sparrows, the high nest-attendance in males even prior to the female s fertile period can be taken as evidence of the great importance of nest-guarding behaviour. Nevertheless, the data suggest that mate-guarding is more important during the fertile period because males frequently leave the nest when the females fly off (Fig. 1b). An alternative explanation for close following behaviour may be the copulatory-access hypothesis (Gowaty and Plissner 1987), whereby males try to maintain contact with their mate to be ready when the female solicits copulation. One prediction of the copulatory-access hypothesis is that the intensity of mate-guarding should stay constant even when the risk of cuckoldry varies. This is not the case in

7 sparrows, as mate-guarding behaviour changes throughout the fertile period with colony size (Fig. 1b, c) as well as with breeding density per site (Fig. 2c). Another possible explanation for mate-guarding is the female-advantage hypothesis. This predicts that the increased proximity is beneficial to the female, either because of reduced harassment from other males (Gowaty and Buschhaus 1998) or increased foraging success, or because of a combination of the two (Lamprecht 1989). This, however, seems unlikely for sparrows, since the majority of following is done by males while females do not change their behaviour throughout the breeding cycle. Why do male sparrows use both paternity guards? One must address the question of why male house sparrows need two paternity guards. One possible explanation is given by the difference in the timing of the two paternity guards according to the social situation: frequent copulations tend to occur relatively earlier in the female cycle when risk of extra-pair copulations is high but the likelihood of a successful fertilisation is low. At the same time, mate-guarding is less intense in the large colony situation, whereas in the small colony or in solitary breeding pairs, where it is less likely that an extra-pair copulation occurs, males adopt the mate-guarding strategy rather than frequent copulations. So, comparing colonies of varying size and solitary breeding pairs revealed that, during the weak fertile period, the two paternity guards appeared to be used alternatively (Fig. 1). This might be connected with the trade-off in nest-guarding versus mate-guarding which has mainly to do with the variation in both female value and risk posed by an extra-pair copulation. However, examination of the same results according to the breeding density per site revealed no such alternative tactic in the weak fertile phase. Actually, both paternity guards (copulation frequency and time a pair spent together) are positively correlated with breeding density during the peak fertile period (Fig. 2). The positive relationship between copulation and mate-guarding in the peak fertile period suggests that some males are able to perform both strategies and others are not. This might also be influenced by nest-site quality. For instance, some males have better nest sites in that they can watch the nest as well as the foraging female from the roof of the building. They can interfere whenever the female is chased or is likely to copulate with another male. Another explanation could be the male s ability to perform efficient mate-guarding and frequent copulations while maintaining other important behaviours like nestguarding and foraging (Sherman and Morton 1988). Møller (1990) pointed out that the size of a male s breast patch is an indicator of his quality, and, indeed, the examination of different morphological traits and male paternity-assurance behaviour revealed that only the breast patches are positively related to both paternity guards. Males in larger colonies have larger patches and paternity guards are related to colony size. The question arises whether paternity guards are only adaptations to the breeding situation or if they are also influenced by male quality. To overcome this problem, the effect of breeding density was controlled, with the result that only mateguarding in terms of the time the male spent near the female seems to be affected by male quality. Copulation frequency, which is generally thought to be the cheaper strategy (Møller and Birkhead 1991) in terms of energy losses, is not reflected in male quality features. One prediction of the trade-off hypothesis (Hasselquist and Bensch 1991) is that males are expected to invest more effort in mate-guarding their females when the probability of attracting a new female is low, usually late in the breeding season. Our results show that the mateguarding did not increase as the breeding season advanced (Table 1). On the contrary, the time spent together tended to decrease as the breeding season advanced. One possible explanation may be that females have fewer opportunities to engage in extra-pair copulations late in the season. In turn, males allocate less time to guarding their females (Pilastro et al. 2002; Griggio et al. 2005; Griggio and Venuto 2007). To conclude, male house sparrows use both paternity guards and fine-tune their strategies according to the time in the female cycle as well as the social situation. Acknowledgments We thank Uwe Römer for assistance in the field. This study was supported by a grant from Österreichische Fonds zur Förderung der Wissenschaftlichen Forschung (No. FWF B17). References Akçay E, Roughgarden J (2007) Extra-pair paternity in birds: review of the genetic benefits. Evol Ecol Res 9: Birkhead TR (1978) Behavioural adaptations to high density nesting in the common guillmot Uria aalge. Anim Behav 26: Birkhead TR (1982) Timing and duration of mate guarding in magpies, Pica pica. Anim Behav 30: Birkhead TR, Møller AP (1992a) Sperm competition in birds: evolutionary causes and consequences. Academic Press, London Birkhead TR, Møller AP (1992b) Numbers and size of sperm storage tubules and the duration of sperm storage in birds: a comparative study. Biol J Linn Soc 45: Birkhead TR, Pellatt J, Hunter FM (1988) Extra-pair copulation and sperm competition in the zebra finch. Nature 334:60 62 Birkhead TR, Wishart GJ, Biggins JD (1995) Sperm precedence in the domestic fowl. Proc R Soc Lond B 261: Briskie JV (1990) Behavioural and anatomical correlates of sperm competition in birds. Ph.D. thesis, Queen s University, Kingston, Canada Colegrave N, Birkhead TR, Lessels CM (1995) Sperm precedence in zebra finches does not require special mechanisms of sperm competition. Proc R Soc Lond B 259:

8 Dawkins R, Carlisle TR (1976) Parental investment, mate desertion and a fallacy. Nature 262: Gladstone DE (1979) Promiscuity in monogamous colonial birds. Am Nat 114: Gowaty PA, Buschhaus N (1998) Ultimate causation of aggressive and forced copulation in birds: female resistance, the CODE hypothesis, and social monogamy. Am Zool 38: Gowaty PA, Plissner JH (1987) Association of male and female American robins (Turdus migratorius) during the breeding season: paternity assurance by sexual access or mate-guarding? Wilson Bull 99:56 62 Griffith SC, Owens IPF, Burke T (1999) Female choice and annual reproductive success favour less-ornamented male house sparrows. Proc R Soc Lond B 266: Griffith SC, Owens IPF, Thuman KA (2002) Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol Ecol 11: Griggio M, Venuto G (2007) The relationship between mate guarding and brood desertion in the rock sparrow Petronia petronia. Ethol Ecol Evol 19: Griggio M, Matessi G, Pilastro A (2005) Should I stay or should I go? Female brood desertion and male counterstrategy in rock sparrows. Behav Ecol 16: Hasselquist D, Bensch S (1991) Trade-off between mate guarding and mate attraction in the polygynous great reed warbler. Behav Ecol Sociobiol 28: Hatchwell BJ, Davies NB (1992) An experimental study of mating competition in monogamous and polyandrous dunnocks Prunella modularis. I. Mate-guarding and copulations. Anim Behav 43: Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev Camb Philos Soc 75:21 64 Kempenaers B, Verheyen GR, Van den Broeck M, Burke T, Van Broeckhoven C, Dhondt AA (1992) Extra-pair paternity results from female preference for high quality males in the blue tit. Nature 357: Lamprecht J (1989) Mate guarding in geese: awaiting female receptivity, protection of paternity or support of female feeding? In: Rasa AE, Vogel C, Voland E (eds) The sociobiology of sexual and reproductive strategies. Chapman & Hall, London, pp Lifjeld JT, Marstein B (1994) Paternity assurance behaviour in the House Martin Delichon urbica. J Avian Biol 25: Møller AP (1985) Mixed reproductive strategies and mate guarding in a semi-colonial passerine, the swallow Hirundo rustica. Behav Ecol Sociobiol 17: Møller AP (1987a) Advantages and disadvantages of coloniality in the swallow Hirundo rustica. Anim Behav 35: Møller AP (1987b) Variation in badge size in male house sparrows Passer domesticus: evidence for status signalling. Anim Behav 35: Møller AP (1987c) House sparrow, Passer domesticus, communal displays. Anim Behav 35: Møller AP (1990) Sexual behaviour is related to badge size in the house sparrow Passer domesticus. Behav Ecol Sociobiol 27:23 29 Møller AP, Birkhead TR (1991) Frequent copulations and mate guarding as alternative paternity guards in birds: a comparative study. Behaviour 118: Møller AP, Birkhead TR (1993) Certainty of paternity covaries with paternal care in birds. Behav Ecol Sociobiol 33: Moreno-Rueda G (2005) Sexual size dimorphism and assortative mating for morphological traits in Passer domesticus. J Ethol 24: Mougeot F (2004) Breeding density, cuckoldry risk and copulation behaviour during the fertile period in raptors: a comparative analysis. Anim Behav 67: Nakagawa S, Ockendon N, Gillespie DOS, Hatchwell BJ, Burke T (2007) Assessing the function of house sparrows bib size using a flexible meta-analysis method. Behav Ecol 18: Norušis MJ (1993) SPSS for windows: Base system user s guide, release 6.0. SPSS, Chicago Pilastro A, Griggio M, Biddau L, Mingozzi T (2002) Extrapair paternity as a cost of polygyny in the rock sparrow: behavioural and genetic evidence of the trade-off hypothesis. Anim Behav 63: Pinxten R, van Elsacker L, Verheyen RF (1987) Duration and pattern of mate guarding in the starling. Ardea 75: Sheldon BC (1994) Timing and use of paternity guards by male chaffinches. Behaviour 129:79 97 Sherman PW, Morton ML (1988) Extra pair fertilizations in mountain white-crowned sparrows. Behav Ecol Sociobiol 22: Summers-Smith D (1954) The communal display of the house sparrow Passer domesticus. Ibis 96: Svensson L (1992) Identification guide to European passerines. British Trust for Ornithology, Thetford Václav R, Hoi H (2002) Importance of colony size and breeding synchrony on behaviour, reproductive success and paternity in house sparrow Passer domesticus. Folia Zool 51:35 48 Václav R, Hoi H, Blomqvist D (2002) Badge size, paternity assurance behaviours and paternity losses in male house sparrow. J Avian Biol 33: Veiga JP, Puerta P (1996) Nutritional constraints determine the expression of a sexual trait in the house sparrow, Passer domesticus. Proc R Soc Lond B 263: Westneat DF, Stewart IRK (2003) Extra-pair paternity in birds: causes, correlates, and conflict. Annu Rev Ecol Evol Syst 34: Wetton JH, Parkin DT (1991) An association between fertility and cuckoldry in the house sparrow Passer domesticus. Proc R Soc Lond B 245: Wittenberger JC, Hunt GL Jr (1985) The adaptive significance of coloniality in birds. In: Farner DS, King JR, Parkes KC (eds) Avian biology, vol 8. Academic Press, Orlando, pp 2 78