Breeding synchrony and paternity in the barn swallow (Hirundo rustica)

The barn swallow (Hirundo rustica) is a socially monogamous passerine which usually breeds in colonies where extra-pair copulations are frequent. Males intensively guard their mates during the female fertile period. Since males are more likely to be available for extra-pair copulations when their mate is not fertile, synchrony in timing of breeding may affect paternity of individual males. In this study, we analysed the change in mate-guarding rate by males in relation to the fertility condition of the female, and the relationships between breeding synchrony and density with paternity in first broods of 52 male barn swallows. Paternity (proportion of nestlings fathered in own brood) was assessed by typing of three highly polymorphic microsatellite loci. Mate guarding by males peaked during the fertile period of their mates. Paternity increased as breeding synchrony in the colony increased. Paternity of barn swallows is positively associated with the degree of exaggeration of male tail ornaments. The relationship between male ornamentation and paternity was partly mediated by an effect of ornament size on breeding synchrony. We suggest that females might delay breeding with low-quality males to enhance their opportunities for being fertilised by high-quality extra-pair males. Received: 16 January 1998 / Accepted after revision: 25 October 1998     

Intraspecific nest parasitism in the swallow Hirundo rustica: the importance of neighbors

Summary Intraspecific nest parasitism in the swallow Hirundo rustica involves several parasite and anti-parasite tactics. Neighboring swallows breed asynchronously, perhaps because neighboring nests with overlapping egg-laying periods have higher frequency of intraspecific nest parasitims than neighboring nests with no such overlap. Since nest guarding prevents nest parasitism, the effect of nest guarding was removed by putting up old swallow nests. Such experimental nests were parasitized by swallows more often when the nests contained eggs, than when empty, and when the nests were far away from, rather than close to, an active neighboring nest. Close experimental nests with eggs were, however, parasitized less frequently if asynchronous (non-overlapping egg-laying periods), rather than synchronous, to active neighboring nests. Aggressive anti-parasite behavior of nest owners was determined from responses towards female intruders. Responses were more often aggressive before and especially during egg laying than during incubation. Nest owners also behaved aggressively more often when the intruder approached close to as compared to at some distance from their nest. Focal pairs behaved aggressively more often towards closely approaching intruders during the incubation period than towards distantly approaching intruders during the egg-laying period. Swallows reduce the frequency of intraspecific nest parasitism by nesting asynchronously with and close to a neighboring nest. Aggression by neighbors may reduce the success of potential parasitic swallows.     

Mixed reproductive strategy and mate guarding in a semi-colonial passerine,the swallow Hirundo rustica

Summary Both male and female swallows Hirundo rustica have a mixed reproductive strategy (parental care for offspring and extra-pair couplations). Mate guarding protects females from male harassment and male swallows from being cuckolded. Females hide their fertile period by copulating successfully with their mates for an extended period during first clutches. Males guard in the pre-fertile period, when many unpaired males are present. Early breeding swallows guard more than late breeders since more sexual chases of females by non-mate males take place in the early period. Solitarily breeding females experience few chases by strange males; copulation frequency, length of copulation period and mate guarding is adjusted to a lower level than among colonial birds. Male guarding activity is more intense in the fertile than in the pre-fertile period. Guarding reduces success of extra-pair copulation attempts.Three female swallows each paired and copulated with a single male and later changed to a new male before starting to breed. Extra-pair copulations most often take place between neighbouring swallows in the fertile period of the female. Many old, early breeding males and many young, late breeding females participate in extra-pair couplations. Successful extra-pair copulations peak in the fertile period contrary to success of pair copulations which does not change during the copulation period.     

Female preference for apparently symmetrical male sexual ornaments in the barn swallow Hirundo rustica

Summary The outermost tail feathers of barn swallows Hirundo rustica apparently reliably signal the quality of males, because individuals with the longest tails have the lowest degree of fluctuating asymmetry (random deviations from symmetry in the otherwise symmetrical tail trait) despite the size of their secondary sexual character. I experimentally tested whether females preferred males with symmetrical tails without altering the aerodynamic properties of birds by painting the tips of the outermost tail feathers with white or black correction fluid. Unmated males were randomly assigned to one of four treatments: (i) asymmetrical tails, where the outermost 20 mm of one tail feather was painted white and the other black; (ii) symmetrical tails where the outermost 10 mm of both tail feathers was painted white (symmetric I); (iii) symmetrical tails where the outermost 20 mm of both tail feathers was painted white (symmetric II); or (iv) controls where the outermost 20 mm of both tail feathers was painted black. The experimental treatment affected the duration of the premating period since it took longer for asymmetrical males to acquire a mate than for either group of symmetrical males or control males. This gave rise to a delayed start of laying among males with apparently asymmetrical tails. The seasonal production of fledglings therefore decreased from control males through males with either symmetrical treatment to males with the asymmetrical treatment. Females therefore pay direct attention to the level of fluctuating asymmetry in secondary sexual characters even when the asymmetry does not affect the aerodynamic properties of males.     

Variation in sperm morphometry and sperm competition among barn swallow (Hirundo rustica) populations

Spermatozoa vary greatly in size and shape among species across the animal kingdom. Postcopulatory sexual selection is thought to be the major evolutionary force driving this diversity. In contrast, less is known about how sperm size varies among populations of the same species. Here, we investigate geographic variation in sperm size in barn swallows Hirundo rustica, a socially monogamous passerine with a wide Holarctic breeding distribution. We included samples from seven populations and three subspecies: five populations of ssp. rustica in Europe (Czech, Italy, Norway, Spain, and Ukraine), one population of ssp. transitiva in Israel, and one population of ssp. erythrogaster in Canada. All sperm traits (head length, midpiece length, tail length, and total length) varied significantly among populations. The variation among the European rustica populations was much lower than the differences among subspecies, indicating that sperm traits reflect phylogenetic distance. We also performed a test of the relationship between the coefficient of between-male variation in total sperm length and extrapair paternity levels across different populations within a species. Recent studies have found a strong negative relationship between sperm size variation and extrapair paternity among species. Here, we show a similar negative relationship among six barn swallow populations, which suggests that the variance in male sperm length in a population is shaped by the strength of stabilizing postcopulatory sexual selection.     

Male tail streamer length predicts fertilization success in the North American barn swallow (Hirundo rustica erythrogaster)

In socially monogamous species, extra-pair paternity has the potential to increase the variance in male reproductive success, thereby affecting the opportunity for sexual selection on male extravagant ornamentation. In the European barn swallow (Hirundo rustica rustica), the tail streamer length is a sexually selected male ornament and an honest indicator of viability. The North American barn swallow (Hirundo rustica erythrogaster) also shows sexual dimorphism in tail streamer length, but whether this trait holds the same signalling function in this subspecies is a controversial issue, and the available literature is presently scarce. Here, we present data on paternity in the North American barn swallow, including a complete sampling of extra-pair sires in four colonies. We analysed how extra-pair paternity affected the variance in male fertilization success and examined whether male tail streamer (i.e. the outermost tail feather) length correlated with fertilization success (n=86 males). Extra-pair paternity constituted 31% of all offspring and significantly increased the variance in male fertilization success. The number of offspring sired by extra-pair males accounted for almost half of the total variance in male fertilization success. Males with naturally long tail streamers had a higher fertilization success than males with shorter tail streamers, and this pattern was mainly caused by a higher extra-pair success for males with long tail streamers. Males with long tail streamers also paired with early breeding females in prime body condition. These results are consistent with the idea that there is directional sexual selection on male tail streamer length, possibly mediated through male extra-pair mating success or the timing of breeding onset.     

Sexual selection, feather breakage and parasites: the importance of white spots in the tail of the barn swallow (Hirundo rustica)

The long outermost tail feathers of barn swallows Hirundo rustica have white spots that are larger in males than in females and in adults than in juveniles. Spot size increases with age among adults and is positively correlated with tail length. We tested the functional significance of these white spots by randomly assigning males to either of three groups during spring: (1) subjected to a considerable reduction in the size of all spots using a black permanent pen; (2) subjected to a small reduction in the size of all spots; or (3) a control group with no reduction. Experimental treatment significantly affected the total number of offspring produced per season: breeding tended to be delayed and second broods were less frequent after a considerable reduction in the size of the males' tail feather spots. White parts of feathers lacking melanin were more often found to be the site of feather breakage than the melanised parts of similar width. Furthermore, white tail spots were the preferred feeding site of feather-eating Mallophaga and, since long-tailed males have fewer Mallophaga than short-tailed males, long-tailed males may pay a lower cost for their large white tail spots than short-tailed males. Hence, the cost of increased risk of feather breakage at white tail spots and the non-random distribution of feather lice among individuals will render tail spots a reliable signal of phenotypic quality. Received: 25 May 1998 / Accepted after revision: 4 January 1998     

Vitamin E supplementation enhances growth and condition of nestling barn swallows (Hirundo rustica)

To optimize fitness, organisms may have to trade the number and quality of individual offspring against their own condition and survival. Limiting micronutrients such as antioxidants may be crucial to this trade-off. We investigated whether vitamin E, a major antioxidant in the diet of vertebrates, is limiting to barn swallow (Hirundo rustica) nestlings. We manipulated brood size to alter the intensity of sib–sib competition and supplemented nestlings with two different physiological doses of vitamin E while establishing a control group. Treatment effects were measured on body mass and size, feather growth, T cell-mediated immune response and hematocrit. Supplementation with vitamin E at intermediate physiological doses improved nestling mass and condition and feather growth, whereas higher physiological doses did not enhance offspring quality compared to a control treatment. The positive effects of vitamin E on body mass and condition were only detectable from days 6 to 10 when maximum growth rate is attained. Experimental enlargement of broods reduced body mass and size and T cell-mediated immune response only during the late nestling period. The effect of vitamin E supplementation did not depend on brood size manipulation, as revealed by the nonsignificant statistical interaction. This result contradicts the hypothesis that availability of vitamin E depends on intrabrood competition and instead suggests that it depends on concentration of vitamin E in the insect prey of swallows. Thus, antioxidants may be available in limited amounts to barn swallow nestlings and such limitation affects growth. In addition, present results confirm that barn swallow parents trade progeny number against growth and immunity of individual offspring.     

Orientation experiments with displaced juvenile barn swallows (Hirundo rustica) during autumn migratory season

In a previous paper, we reported that juvenile barn swallows (Hirundo rustica) trapped during the autumn migratory season and tested in modified Emlen funnels under overcast conditions can use magnetic information for compass orientation, although they did not orient toward the expected migratory direction. To further investigate this behaviour, in the present paper, we report the results of two series of displacement experiments performed on juvenile barn swallows belonging to two different roost sites [Massaciuccoli Lake (ML) and Terzo Cavone (TC)] and tested using the same protocol as that previously adopted. On the whole, the outcome of the ML and TC experiments was quite different with respect to (a) the degree of bird activity within the funnel (substantially lower for TC) and (b) the effect of the experimental displacement on the directional preferences of the tested subjects (not detectable in TC, while evident in ML swallows). Taken together, these results suggest that migrating swallows could react differently to the experimental tests depending on the roost site where they were caught. Indeed, TC swallows, trapped in southern Italy, close to the seacoast, and characterized by fairly large amounts of fat stores, mainly broke off their migratory activity or reoriented their directional preferences toward inland sites, possibly in search of more profitable habitats. On the other hand, ML swallows, trapped about 660 km to the north and characterized by lower amounts of fat stores, apparently tried to compensate for the experimental displacement.

Settlement patterns of female barn swallows Hirundo rustica across different group sizes: access to colorful males or favored nests?

In most avian species, individuals are faced with two critical decisions at the start of a breeding season: choosing a breeding site and a mate. An analysis of these decisions in light of population-level patterns, such as group size variation in social breeders, can illuminate the causes and patterns of habitat selection behavior. Group sizes are variable in barn swallows; however, no clear and consistent benefits of group breeding have been found in this species, and it is puzzling as to why individuals breed socially. Previous analyses demonstrated that individuals aggregate to gain access to nests that were constructed during previous seasons; however extra-pair matings are also prevalent in this species, raising questions about the mate-selection strategies of females across different group sizes. In this paper, I address the question of how females make their first site-selection decisions in terms of two features known to be causally related to seasonal reproductive success: (1) colorful males or (2) old nests. Using experimental and observational data, I tested, but found no support for, the hypotheses that propose female settlement decisions are a function of (1) the prevalence of colorful males or (2) the increased opportunity for extra-pair matings at group sites. Instead, it is apparent that female settlement patterns are strongly tied to the availability of old nests at a site. Extra-pair fertilizations are equally common across all group sizes in this population, suggesting that females do not face a trade-off between old nests and the possibility of extra-pair mating decisions when making settlement decisions.     

Mate guarding in the swallowHirundo rustica

Summary The importance of mate guarding by males in the monogamous swallowHirundo rustica was studied by temporarily detaining the males. Mate guarding reduced the frequency of extra-pair copulations and of sexual chases involving female mates. Males participated in sexual chases more frequently if they had a non-fertile female. Neighbouring males of ‘widowed’ females increased their own mate guarding presumably in response to the experimentally increased rate of sexual chases. Neighbouring males with a fertile female increased their mate guarding more than did males with a non-fertile female. Addition of eggs to swallow nests in the post-fledging period of the first brood induced mate guarding by male nest owners. These males also copulated more frequently with their mates than did control males. Neighbouring male swallows responded to the increased mate guarding by showing sexual interest in the guarded females. removal of eggs from swallow nests during the laying period, leaving only one egg in the nest, resulted in reduced nest attendance by females. Male mates responded by increasing their mate guarding intensity as compared to controls, and neighbouring males showed an increased sexual interest in these females.     

Foraging costs of a tail ornament: Experimental evidence from two populations of barn swallows Hirundo rustica with different degrees of sexual size dimorphism

Secondary sexual characters are assumed to be costly to produce or maintain. A test of this assumption was performed using the sexually exaggerated outermost tail feathers of male barn swallows Hirundo rustica, a trait currently subject of a directional female mate preference. A possible cost of sexual signalling in male barn swallows arises from increased flight cost during foraging in this aerially insectivorous species. A longer tail may impose a greater drag during flight and thereby affect foraging ability. This was tested by determining the relationship between experimentally modified male tail lengths and number and size of prey delivered to offspring in Spain, where sexual size dimorphism in tail length is small, compared to Denmark, where dimorphism is large. Food boluses contained significantly fewer small insects in Spain than in Denmark. Males with elongated tails captured more and smaller insects while males with shortened tails captured fewer and larger prey items at both sites. Males with naturally long tails were less affected by experimental treatment in terms of effects on the number and the size of prey delivered to their offspring, a finding consistent with a long tail being a condition-dependent viability indicator. The effect of a given degree of tail manipulation on prey size and number of prey per bolus was larger in Spain than in Denmark. These results demonstrate that (1) tail length in male barn swallows affects foraging, and (2) larger sexual size dimorphism occurs where the foraging cost of an increment in ornament size is smallest.Communicated by M. Zuk     

Parent-absent signalling of need and its consequences for sibling competition in the barn swallow

In species with parental care, competition among siblings for access to limited parental resources is common. Sibling competition can be mediated by begging behaviour, a suite of different visual and acoustic displays by which offspring solicit parental care. These are mostly addressed to the parents upon food provisioning, but can also be performed in the absence of the attending parents. This so-called parent-absent begging (PAB) may function as an intrabrood communication signal and potentially affect intrabrood competition dynamics for access to food. We investigated the role of PAB in moulding sibling interactions and its effect on food intake among altricial barn swallow (Hirundo rustica) nestlings, both under normal and experimentally reduced food intake. Frequency of PAB increased after food deprivation. Nestlings that had performed PAB increased their begging intensity upon the subsequent parental feeding visit, while siblings reduced their own begging level, but only when they had not been food-deprived. As a consequence, nestlings which had performed PAB before parental arrival had larger chances of receiving food. However, nestlings did not benefit from displaying PAB when competing with food-deprived siblings. Our findings show that PAB reliably reflects need of food, indicating that a nestling will vigorously compete for the subsequent food item. By eavesdropping siblings' PAB displays, nestlings may optimally balance the costs of scrambling competition, the direct fitness gains of being fed and the indirect fitness costs of subtracting food to needy kin. However, large asymmetries in satiation between competitors may lead individual offspring to monopolize parental resources, irrespective of PAB displays.     

Occurrence of extra-pair copulation in the tree swallow (Tachycineta bicolor)

Summary A new method to mark sperm transfer events between birds, using microspheres inserted into males' cloacae, was employed to assess the frequency of extra-pair copulation (EPC) in a population of tree swallows (Tachycineta bicolor) in Ontario, Canada, during the summer of 1988. We inserted 25 males with microspheres; spheres from 8 (32%) of these males were found in extra-pair females, from which we infer that males pursue a mixed reproductive strategy of monogamy coupled with seeking EPCs. The cloacae of 10 of 41 (24.4%) females were found to contain microspheres from non-mates. EPCs occur more frequently between neighboring birds than between non-neighbors. Only two within-pair copulations were detected with this method, suggesting that it underestimates the occurrence of all copulations, extra-pair or within-pair. Copulation watches revealed that within-pair copulations occur very frequently. We propose that frequent pair copulations are used by males to ensure their paternity in their mate's offspring. Offprint requests to: R.J. Robertson     

Solicitation displays reliably reflect oxidative damage in barn swallow nestlings

Reproduction entails parental decisions over allocation of limiting resources. ‘Begging’ solicitation displays by the offspring have been hypothesised to evolve as reliable indicators of quality, allowing parents to adopt optimal allocation strategies. To function as such, however, begging signals must covary with offspring traits that affect viability. Here we tested whether oxidative damage of nestling barn swallows predicts begging bout duration, call amplitude and intensity of postural displays both under normal food provisioning and under food shortage. Oxidative damage as determined by normal metabolism, pathological conditions and functioning of the immune system can serve as a comprehensive indicator of offspring condition because it can profoundly affect viability, senescence and reproduction. Begging bout duration was negatively predicted by oxidative damage but only after food deprivation. Postural begging negatively covaried with oxidative damage, at least when nestlings were confronted with related nest mates. Plasma antioxidant capacity did not predict begging behaviour. Thus, we show for the first time that behavioural begging covaries with a comprehensive index of chick condition, lending support to reliability of such begging traits also as signals of quality rather than need or hunger only. Future studies are candidate to decouple the effect of hunger state and individual condition on behavioural begging.     

Extra-pair paternity and the reproductive role of male floaters in the tree swallow (Tachycineta bicolor)

In many avian species, a part of the population is present at the breeding grounds but does not breed. Current theories generally assume that floaters are younger or lower-quality individuals, and empirical data confirm this. However, floating could also arise as an alternative strategy to breeding, if floaters are able to reproduce via extra-pair copulations. Until the present study, there has been no evidence that floaters father offspring. We studied a population of tree swallows (Tachycineta bicolor), a species with one of the highest levels of extra-pair paternity known in birds. Using microsatellite markers, we determined the biological fathers of 65% of the extra-pair young. Of a total of 53 extra-pair young (52% of all offspring), 47% were fathered by local residents, 6% by residents breeding elsewhere (up to 2 km from the focal grid), and 13% by floaters. Residents seemed to be more successful and they were also more likely to return as territory holders in the next breeding season compared to floaters. Extra-pair males were on average in better condition than the within-pair males they cuckolded. Interestingly, resident males that disappeared (possibly to float) during the fertile period were heavier than males that stayed, and floaters were heavier than residents, but not different in any other characteristic. Although alternative interpretations of the data are possible, we propose that floating might be a conditional strategy in tree swallows whereby males in good condition gain more paternity via extra-pair copulations, whereas males in worse condition are more successful by providing parental care.     

Sex-related asymmetry in competitive ability of sexually monomorphic barn swallow nestlings

In diverse taxa, offspring solicit parental care using complex displays, which may evolve as reliable signals of condition or as mechanisms to manipulate parental investment. Differential sex allocation may therefore result from adaptive parental decisions or sex-related variation in competitive ability or because of sex-related asymmetries in kin selection. Under normal food provisioning, female barn swallow (Hirundo rustica) nestlings begged more loudly but did not receive more food than male nestlings. After food deprivation, begging call loudness of males but not females increased. Begging loudness positively predicted the number of feedings received by the nestlings, and males gained more mass than females after food deprivation. Male nestlings are more severely affected by chronic food reduction and may therefore accrue a larger benefit compared to females by increasing their food intake under short-term conditions of food scarcity. These results suggest that either females do not increase begging intensity to favour male broodmates which are more vulnerable to prolonged food stress, or that males prevail in scramble competition despite being similar in size to females.     

Individual and environmental determinants of reproductive success in male tree swallow (Tachycineta bicolor)

Evaluating the contribution of individual and environmental determinants of reproductive success is essential to improve our understanding of sexual selection. In socially monogamous bird species with high rates of extrapair paternity, traits or environmental contexts affecting the number of within-pair young (WPY) produced by males can differ from those affecting the number of extrapair young fathered (EPY). Here, we use a 4-year dataset collected in contrasted environments to assess the factors affecting male reproductive success in tree swallows (Tachycineta bicolor), a species showing high levels of extrapair paternity. Our analyses revealed that the number of WPY was higher under better environmental conditions, while the number of EPY was mainly related to male characteristics. Males nesting in more intensive agricultural areas had fewer WPY produced and a lower reproductive success. Also, males breeding earlier in the season had more WPY. The presence of parasites reduced males’ reproductive success, mainly by reducing the number of EPY. The influence of male phenotype varied according to population density: Tarsus length variation had a greater effect on reproductive success at low population density than at high density, while wing length was also positively related to the number of EPY, more so at high than at low density. Altogether, our results suggest a complex interplay between individual and environmental determinants of reproductive success and imply that sexual selection dynamics varies depending on environmental contexts.     

Testosterone-induced depression of male parental behavior in the barn swallow: female compensation and effects on seasonal fitness

In birds, many aspects of male socio-sexual and parental behavior are influenced by androgens, most notably testosterone (T). We report the effects of subcutaneous T-implants in male barn swallows (Hirundo rustica) on male and female parental behavior and on seasonal reproductive success. Males were assigned to one of three experimental groups: (i) implanted with a T-filled Silastic tube; (ii) implanted with an empty Silastic tube; and (iii) not implanted. T-implanted males provided a smaller proportion of feedings (number of feedings by the male/total number of feedings by both parents) and fed nestlings less frequently (number of feedings/h) than males of the other two groups. Females paired to T-implanted males fed nestlings significantly more often than females paired with unimplanted males. Females almost fully compensated for their mates' shortfall, and this resulted in similar combined feeding efforts among treatments. Reproductive success in their first broods or during the entire breeding season was unaffected by T- treatment. These results confirm earlier reports of the suppressive effects of T on male parental behavior. However, they are inconsistent with current ESS models that predict partial compensation as the optimal response by one individual to reduction of parental effort by its mate in monogamous, biparental systems.     

Timing of arrival from spring migration is associated with flight performance in the migratory barn swallow

Timing of arrival at the breeding grounds by migratory birds affects their mating success and access to superior resources, thus being a major factor associated with fitness. Much empirical work has been devoted to investigate the condition dependence of arrival sequence of migrants and characteristics of individuals that influence arrival time from migration. Surprisingly, there are no studies examining the relationship between flight performance of individual birds and their arrival time. I investigated the relative importance of direct effects of short-term flight performance, age, body condition and the degree of sexual ornamentation (tail length) on timing of spring arrival in the barn swallow (Hirundo rustica), a long-distance trans-equatorial passerine migrant. I evaluated short-term flight performance (a composite variable comprising flight manoeuvrability, velocity and acceleration) in a standardised manner using flight tunnels. Short-term flight performance was a significant and important predictor of spring arrival date. Furthermore, locomotion predicted arrival date of individual birds independently of morphological variables—the degree of sexual ornamentation (the length of the tail) and wing aspect ratio and body condition. I discuss the possible role short-term flight performance may have in determining migratory performance. This is the first time flight performance has been shown to be associated with timing of arrival from migration in a migratory bird.