Parent-offspring recognition in the barn swallow (Hirundo rustica)

Past research has shown that in the colonial bank swallow and cliff swallow, parents and offspring recognize one another by calls, enabling parents to locate and feed only their own chicks. To test the hypothesis that recognition traits are adaptations to coloniality, we examined parent-offspring recognition in the related but non-colonial species, the barn swallow. To allow cross-species comparisons, we used the same methods that had been used in the previous swallow studies. We carried out four studies. (1) Cross-fostering experiments done immediately before fledging gave no evidence of recognition. (2) In a playback experiment, parents gave no indication that they recognized the calls of their offspring. (3) In another playback experiment, chicks responded more strongly to the calls of their parents than to the calls of unrelated adults. The degree of recognition, however, was somewhat weaker than that seen in the two colonial swallow species. (4) Newly fledged young did not creche after fledging. Rather, family groups generally stayed apart from one another for almost 2 weeks, while parental care was still being given. The comparative data suggest that parent-offspring recognition via individually distinctive cues evolved in response to the intermingling of young associated with colonial living, and it thus weakly expressed in barn swallows compared to cliff swallows and bank swallows.     

Ectoparasites and reproductive trade-offs in the barn swallow (Hirundo rustica)

Parents are predicted to trade offspring number and quality against the costs of reproduction. In altricial birds, parasites can mediate these costs because intensity of parasitism may increase with parental effort. In addition, parasites may mediate a trade-off between offspring number and quality because nestlings in large broods may have reduced anti-parasite immune defence. In this study, we experimentally analysed the effect of brood size on infestation by an ectoparasitic mite in nests of barn swallows (Hirundo rustica). Nests with an enlarged brood had larger prevalence and intensity of infestation than those with a reduced brood. Importantly, each nestling in enlarged broods was exposed to a larger number of mites, even when measured on a per nestling basis, than in reduced broods. Nestlings in enlarged broods had smaller body mass and T-cell-mediated immune response compared to reduced broods. T-cell-mediated immune response and feather growth were negatively correlated with per nestling intensity of infestation in enlarged but not in reduced broods. The results suggest that nestlings in enlarged broods have depressed immunity leading to larger per nestling mite infestation. Hence, exposure to parasites of offspring and parents increases with brood size, and parasitism can thus mediate trade-offs between reproduction and number and quality of the progeny in the barn swallow.     

Energetic cost of tail streamers in the barn swallow (Hirundo rustica)

Different hypotheses stress the importance of natural or sexual selection to explain the evolution and maintenance of long outermost tail feathers in the barn swallow (Hirundo rustica). Since energy costs are predicted to arise from tail length manipulation, we measured the daily energy expenditure in three experimental groups (tail-shortened, tail-elongated, and control birds) with the doubly labelled water technique. Though we did not directly measure flight cost, we assumed this to be positively related to daily energy expenditure. Mass independent daily energy expenditure (kJ/mass^0.67 day) average daily metabolic rate (ml CO₂/g h), and water flux (ml H₂O/g day) did not show any significant difference among treatments in either sex. Males had higher values than females for the three parameters. Males with short original tail length experienced a higher water flux than originally long-tailed males. Females that laid more eggs during the breeding season or had heavier broods also showed higher levels of water flux which could imply a higher food intake. Our expectation of finding energetic costs of manipulated tail length in barn swallows with an integrated measure of metabolism was not fulfilled, and we did not find evidence for behavioural changes in the birds involved in the experiment.     

Gape coloration reliably reflects immunocompetence of barn swallow (Hirundo rustica) nestlings

In some passerines, parents allocate more food to offspringwith the brightest red gapes, but the function of parental decisionsbased on offspring gape coloration is unknown. We hypothesizethat gape coloration is part of a communication system wherenestlings reveal their condition to attending parents, whichmay thus base their decisions on reliable signals of offspringreproductive value. We analyze the effects of brood size manipulation,injection with an immunogen and food deprivation, on gape coloration,morphology, and T-cell–mediated immunocompetence of nestlingbarn swallows (Hirundo rustica). For each gape we measured threecomponents of coloration (hue, saturation, and brightness) andobtained an overall color score by principal component analysis.Enlargement of brood size and injection with an antigen resultedin less red and less saturated and brighter gape color. Nestlingsin enlarged broods had smaller body mass and T-cell–mediatedimmunocompetence compared to those in reduced broods. A positivecovariation existed between redness and saturation of gape colorand T-cell–mediated immunocompetence. Gape color siblingsraised in different nests did not depend on parentage. Thus,condition-dependent gape coloration can reveal different componentsof nestling state on which parents may base their adaptive decisionsabout allocation of care to the offspring.     

Phenotypic quality and molt in the barn swallow, Hirundo rustica

Phenotypic quality may determine the development and expressionof secondary sexual characters. We studied the relationshipbetween molt and several measures of phenotypic quality in thesexually size-dimorphic barn swallow (Hirundo rustica) in itswinter quarters in Namibia. Males were in a more advanced stageof molt than females and juveniles, and the speed of molt asdetermined from the residual of the regression of the size ofthe gap in wings caused by missing and growing feathers on wingmolt score (residual wing raggedness) was also higher in malesthan in females and juveniles. Male barn swallows with longand symmetric tail feathers had a more advanced stage of moltand molted at a higher speed than males with short and asymmetrictails. Long-tailed females had a delayed molt, and females withasymmetric tails had less advanced molt and lower rates of feathergrowth than females with symmetric tails. Molt of secondariesin juveniles also appeared to be less advanced if they had longtails. Adult barn swallows molted their tail feathers in anirregular sequence with the longest, outermost tail featherusually replaced before the second or the third outermost feathers.Good body condition was positively associated with a high moltscore for some feather tracts and a rapid wing molt in adultfemales and tail molt in juveniles. Mallophaga were only weaklynegatively associated with primary and secondary molt scorein adult females and speed of wing molt in adult males. In conclusion,phenotypic quality of adult male barn swallows as reflectedby the expression of their secondary sexual character duringthe previous molt reliably reflected stage and speed of currentmolt.     

Structural coloration and sexual selection in the barn swallow Hirundo rustica

Structural coloration has been hypothesized to play a role insexual selection, and we tested whether this was the case ina field study of the barn swallow Hirundo rustica. The dorsaliridescent plumage of barn swallows has a strong reflectancein the ultraviolet (UV) region, with adult males on averagereflecting 8-9% more than adult females, as revealed by a 2-yearstudy in southwestern Spain. The correlation between structural coloration (described by the reflectance in the UV part of thespectrum, UV chroma and blue chroma) and three other secondarysexual characters significantly associated with male matingsuccess (tail length, tail asymmetry, and red facial coloration)was weak and generally nonsignificant. Nor was there a significantrelationship between color parameters and body condition. Wetested for an association between structural coloration of the dorsal plumage and sexual selection in a number of independenttests. Arrival date of males was not significantly relatedto color; there was no significant relationship between colorationand probability of survival or age; mated males did not havestronger reflectance than unmated males; and the duration ofthe premating period was not significantly related to color.Reproductive success was not significantly correlated withplumage coloration in males, nor was the feeding rate of offspringby brightly colored males higher than that of males with lessbright plumage. Given that sample sizes were large, and the power of statistical tests high, we conclude that current sexualselection on the coloration of the dorsal plumage in the barnswallow is, at best, weak.     

Feather holes and flight performance in the barn swallow Hirundo rustica

Feather holes are small (0.5–1?mm in diameter) deformities that appear on the vanes of flight feathers. Such deformities were found in many bird species, including galliforms and passerines. Holey flight feathers may be more permeable to air, which could have a negative effect on their ability to generate aerodynamic forces. However, to date the effects of feather holes on flight performance in birds remained unclear. In this study we investigated the relationship between the number of feather holes occurring in the wing or tail feathers and short term flight performance traits – aerial manoeuvrability, maximum velocity and maximum acceleration – in barns swallows, which are long distance migrating aerial foragers. We measured short-term flight performance of barn swallows in a standardized manner in flight tunnels. We found that acceleration and velocity were significantly negatively associated with the number of holes in the wing flight feathers, but not with those in the tail feathers. In the case of acceleration the negative relationship was sex specific – while acceleration significantly decreased with the number of feather holes in females, there was no such significant association in males. Manoeuvrability was not significantly associated with the number of feather holes. These results are consistent with the hypothesis that feather holes are costly in terms of impaired flight. We discuss alternative scenarios that could explain the observed relationships. We also suggest directions for future studies that could investigate the exact mechanism behind the negative association between the number of feather holes and flight characteristics.     

Impact of miniaturized geolocators on barn swallow Hirundo rustica fitness traits

Miniaturized light‐level geolocators may revolutionise the study of avian migration. However, there are increasing concerns that they might negatively affect fitness. We investigated the impact of two miniaturized geolocator models (SOI‐GDL2.10, deployed in 2010, and SOI‐GDL2.11, deployed in 2011) on fitness traits of the barn swallow Hirundo rustica, one of the smallest migratory species to which geolocators have been applied to date. The 2011 model was lighter (by 0.09 g) and had a shorter light stalk compared to the 2010 model. Using data from 640 geolocator and 399 control individuals from three geographical populations, we found that geolocators reduced annual survival probabilities (control birds: 0.19–0.63; geolocator birds: 0.08–0.40, depending on year, sex, and how birds that lost the device were considered), with more markedly negative effects on females equipped with the 2010 model. In addition, among birds equipped with the 2010 model, onset of reproduction in the subsequent year was delayed (by 12 d) and females laid smaller first clutches (by 1.5 eggs, i.e. a 30% reduction) compared to controls. Equipping parents with geolocators while they were attending their brood did not affect nestling body mass or fledging success. A reduction of geolocator weight and drag by shortening the light stalk slightly enhanced the survival of females but not that of males, and mitigated the negative carry‐over effects on subsequent reproduction. Our study shows that geolocators can have a negative impact on survival and reproduction, and that even minor differences in weight and drag can make the difference. We suggest that studies aiming at deploying geolocators or other year‐round tagging devices should be preceded by pilot experiments to test for fitness effects.     

Morphological and genetic predictors of parental care in the North American barn swallow Hirundo rustica erythrogaster

Sexually dimorphic traits often signal the fitness benefits an individual can provide to potential mates. In species with altricial young, these signals may also predict the level of parental care an individual is expected to provide to shared offspring. In this study, we tested three hypotheses that traditionally relate sexually dimorphic traits to parental care in two populations of North American barn swallows Hirundo rustica erythrogaster. The good parent hypothesis predicts a positive relationship between an individual's ornamentation and his or her care whereas the differential allocation (more care given by individuals when paired to high quality mates) and reproductive compensation (more care given by individuals when paired to low quality mates) hypotheses predict that an individual's level of parental investment is relative to the quality of their mate. Male and female North American barn swallows have colorful ventral feathers and elongated tail streamers, but there is evidence that ventral color, not tail streamer length, predicts measures of seasonal reproductive success. Accounting for the positive correlation between within‐pair feeding rates and other potentially confounding variables in all of our models, we found no support for the good parent hypothesis because in both males and females, traits shown to be under sexual selection did not predict feeding rates in either sex. However, our data reveal that male coloration, and not streamer length, predicted a female's provisioning rate to shared offspring (females fed more when paired with darker individuals) in two separate populations, supporting the differential allocation, but not the reproductive compensation hypothesis. Because genetic traits have also been shown to affect parental investment, we evaluated this variable as well and found that a male's paternity did not have significant effects on either male or female feeding rates. Overall, our results suggest that females do not pair with darker males in order to gain direct benefits in terms of his expected levels of parental care to shared offspring, but do themselves invest greater levels of care when paired to darker males. Further, our results are consistent with previous studies which suggest that ventral feather color, not streamer length, is a target of sexual selection in North American populations of barn swallow because females invested more in their offspring when paired to darker mates.     

Yolk androgens in the barn swallow (Hirundo rustica): a test of some adaptive hypotheses

Maternal effects such as androgen in avian eggs can mediate evolutionary responses to selection, allowing manipulation of offspring phenotype and promoting trans-generational adaptive effects. We tested the predictions of two adaptive hypotheses that have been proposed to explain female variation in yolk androgen allocation in birds, using the barn swallow Hirundo rustica as a model. We found no support for the first hypothesis proposing that yolk androgen varies as a function of breeding density in order to prepare offspring for different breeding densities. However, we found experimental support for the hypothesis that female yolk androgen allocation depends on mate attractiveness and that it constitutes an example of differential allocation. Females increased the concentration of androgens in their eggs when mated to males with experimentally elongated tails. Female phenotypic quality as measured by arrival date and clutch size was positively related to egg androgen concentration, consistent with the hypothesis that this is a costly investment, constrained by female condition. We found correlative evidence of a direct relationship between egg androgen concentration and performance of offspring as measured by mass increase.     

Development of fluctuating asymmetry in tail feathers of the barn swallow Hirundo rustica

Fluctuating asymmetry represents usually small, random deviations from symmetry in bilateral morphological characters. The ontogeny of asymmetry in morphological characters may reveal information about developmental processes in a general sense. I studied the development of fluctuating asymmetry in feather characters of the barn swallow Hirundo rustica, that are developed repeatedly during the single annual moult, with the following results. First, the side developing a larger feather was found to be partially biased, as demonstrated by one side consistently developing a larger feather under natural and experimentally induced growth episode events. Second, asymmetric feathers were found to consist of asymmetric daily growth increments, and the size of the increments developing under different environmental conditions were positively correlated. Third, fluctuating asymmetries of feathers developing under different environmental conditions were positively correlated, although the level of asymmetry was larger under adverse environmental conditions. Fourth, individual asymmetries in tail length and growth bar length were unrelated to the duration of the developmental period, although late growth increments were smaller and more symmetric than early increments. These observations suggest that fluctuating asymmetry partially arises as a consequence of a random bias in the feather follicles and differences in environmental conditions during ontogeny of feathers.     

Sexual selection in the barn swallow Hirundo rustica. VI. Aerodynamic adaptations

Secondary sexual characters are assumed to be costly to produce and maintain, and this will select for morphological modifications that reduce the magnitude of such costs. Here we test whether a feather ornament, the sexually exaggerated outermost tail feathers of male barn swallows Hirundo rustica, a trait currently subject to a directional female mate preference, and other aspects of the morphology used for flight have been modified to increase aerodynamic performance. This was done by making comparisons among sexes within populations, among individuals varying in tail length within populations, and among populations from different parts of Europe. Male barn swallows experienced reduced drag from their elongated tail feathers by morphological modifications of the ornamental feathers as compared to females. Morphological features of the outermost tail feathers were unrelated to tail length in both males and females within populations. Wing and tail morphology (length of central tail feathers and wings, wing span, wing area, wing loading, and aspect ratio) was modified in males compared to females. Barn swallows with long tails had morphological tail and wing modifications that reduced the cost of a large ornament, and similar modifications were seen among populations. The costs of the exaggerated secondary sexual character were therefore reduced by the presence of cost-reducing morphological modifications. The assumptions of reliable signalling theory, that signals should be costly, but more so to low than to high quality individuals, were not violated because long-tailed male barn swallows had the largest cost-reducing morphological characters.     

Population genetics and morphological comparisons of migratory European (Hirundo rustica rustica) and sedentary East-Mediterranean (Hirundo rustica transitiva) barn swallows

Speciation processes are largely determined by the relative strength of divergent selection versus the magnitude of gene flow. The barn swallow (Hirundo rustica) has a broad geographic distribution that encompasses substantial geographic variation in morphology and behavior. The European (H. r. rustica) and East-Mediterranean (H. r. transitiva) subspecies are closely related, despite differing in morphological and life-history traits. To explore patterns of genetic differentiation and gene flow, we compared morphological and genetic variation among the nonmigratory breeding population of H. r. transitiva from Israel and the migratory population of H. r. rustica that passes through Israel and compared it with the genetic differentiation between H. r. transitiva from Israel and a breeding population of H. r. rustica from the United Kingdom that uses a different migratory flyway. Mitochondrial haplotype network analysis suggests that the European and East-Mediterranean populations are intermixed, although there was low but significant genetic differentiation between the subspecies based on both mitochondrial (F(ST) = 0.025-0.033) and microsatellite (F(ST) = 0.009-0.014) loci. Coalescent-based analyses suggest recent divergence and substantial gene flow between these populations despite their differences in morphological and behavioral traits. The results suggest that these subspecies are undergoing a differentiation process in the face of gene flow, with selection possibly operating on sexually selected traits.     

Microsatellite markers isolated from barn swallows (Hirundo rustica)

Fifteen polymorphic microsatellite DNA loci were isolated from barn swallow (Hirundo rustica) and optimized for future studies of radiation‐induced mutations in populations from Ukraine. The loci were screened for variability among 25 individuals from two populations. The primers amplified loci with relatively high numbers of alleles ranging from five to 32 alleles per locus and polymorphic information content from 0.481 to 0.951. Observed heterozygosity varied from 0.458 to 0.960. None of the loci showed deviations from Hardy–Weinberg equilibrium in either population.     

Sexual selection in the barn swallow (Hirundo rustica). V. Geographic variation in ornament size

Models of sexual selection in a cline predict the patterns of clinal variation in female mate preference and male secondary sexual characters. These predictions were tested for the nominate subspecies of the barn swallow Hirundo rustica which demonstrates clinal variation in morphology, with several characters in both sexes showing increasing size at higher latitudes. Sexual size dimorphism in the length of the tail ornament and the short, central tail feathers increase with increasing latitude while size dimorphism in other morphological characters is independent of latitude. The main reason for the two divergent patterns of sexual size dimorphism appears to be the higher foraging cost of having a long tail ornamental at low latitudes. The control of development decreases with increasing latitude as demonstrated by an increasing latitudinal cline in fluctuating asymmetry of tail length. Phenotypic variance in tail length increases with latitude in males, but not in females, as shown by the coefficients of variation. Clinal variation in morphology is not due to natural selection associated with a latitudinal increase in the distance between breeding and wintering areas. The geographic patterns of morphological variation suggest that the tail character has diverged geographically as a result of a sexual process of reliable signalling.     

The effects of radiation on sperm swimming behavior depend on plasma oxidative status in the barn swallow (Hirundo rustica)

Sperm are highly susceptible to reactive oxygen species (ROS) that can damage sperm DNA and structure, resulting in reduced fertilizing capacity. Exposure to radioactive contamination can also impair sperm swimming behavior and fertilizing ability, both through a reduction of sperm DNA integrity and via an increased generation of reactive oxygen species (ROS). However, the relationship between individual oxidative status and sperm swimming behavior has never been investigated in any wild population of animals exposed to radioactive contamination. We studied the motility of sperm collected from barn swallows, Hirundo rustica, breeding under different levels of radioactive contamination following the Chernobyl accident in 1986, in relation to individual oxidative status. We tested the hypothesis that the degree of impairment of sperm swimming behavior by radioactive contamination depended on plasma antioxidant capacity, the level of reactive oxygen metabolites (ROMs) and oxidative stress (sensu Costantini et al. 2006), a better oxidative status being associated with higher sperm motility. Sperm behavior parameters were subjected to principal component (PC) analysis, which extracted four PCs explaining 86% of the variance in sperm motility. PC2, representing sperm with high track velocity and ample lateral head displacement, was significantly predicted by the interaction between radiation level and either oxidative damage or oxidative stress. Contrary to our predictions, the highest values of PC2 were associated with relatively high radiation levels, particularly for high levels of either ROMs or oxidative stress. In addition, there was a tendency for values of PC3 (representing the percent of motile sperm) and PC4 (representing slow sperm with high beat cross frequency) to depend on the interaction between radiation level and total plasma antioxidant protection. Our results confirm the importance of oxidative status in determining the genetic and physiological outcome of exposure to radioactive contamination, complementing previous studies relating sperm abnormality to circulating levels of specific antioxidants. Our results also complement previous evidence that oxidative damage of sperm was negatively related to sperm motility, thus indicating a possible trade-off in quenching pro-oxidant compounds in the plasma and the seminal fluid.     

Latency in response of barn swallow Hirundo rustica populations to changes in breeding habitat conditions

Inclusion of past, in addition to current ecological conditions can improve the realism of animal‐habitat models, because populations may show delayed responses to changing environments. We studied the relationships between the distribution of barn swallows (Hirundo rustica L.) in 2001 and ecological factors between 1986 and 2001. Livestock farming was the best predictor of swallow distribution. Maximum predictive power of swallow abundance was achieved by livestock farming data 7 years before the census and significantly earlier than 2001, as shown by a bootstrap analysis. Breeding philopatry, social facilitation of breeding habitat choice may delay response of barn swallow populations to rapidly changing ecological conditions in anthropogenic habitats. By bootstrapping the set of farms and applying our predictive distribution models to livestock farming data in the past and those predicted for the near future we forecast no significant change in swallow populations until 2015. This study suggests that population studies should incorporate historical ecological data.     

Sexual selection in the monogamous barn swallow (Hirundo rustica). II. Mechanisms of sexual selection

Mechanisms of sexual selection in the monogamous, sexually dimorphic barn swallow (Hirundo rustica) were studied during a seven-year period. First, the sex ratio of reproducing adults was male-biased, and mated males had significantly longer tail ornaments than unmated males. Secondly, some of the unmated individuals later committed infanticide and became mated with the mother of the killed brood. Fathers of killed broods had significantly shorter tails than other males, and there was a tendency for infanticidal males to have longer tail ornaments than other unmated males. Thirdly, long-tailed male barn swallows were more successful in acquiring extra-pair copulations than other males, and females involved in extra-pair copulations, as compared to females not involved in such copulations, had mates with shorter tail ornaments. Fourthly, male barn swallows having long tails as compared to short-tailed males acquired mates in better body condition. Females mated to long-tailed males reproduced earlier, laid more eggs and were more likely to have two clutches than were females mated to short-tailed males. Finally, females mated to long-tailed males put more effort into reproduction than did other females, as evidenced by their relatively larger contribution to feeding of offspring. Thus, at least five different components of sexual selection affected male reproductive success. Selection arising from differential success during extra-pair copulations, differential reproductive success and differential male reproductive effort thus accounted for most of the selection on tail ornaments in male barn swallows.     

Sex allocation according to multiple sexually dimorphic traits of both parents in the barn swallow (Hirundo rustica)

Parents should differentially invest in sons or daughters depending on the sex‐specific fitness returns from male and female offspring. In species with sexually selected heritable male characters, highly ornamented fathers should overproduce sons, which will be more sexually attractive than sons of less ornamented fathers. Because of genetic correlations between the sexes, females that express traits which are under selection in males should also overproduce sons. However, sex allocation strategies may consist in reaction norms leading to spatiotemporal variation in the association between offspring sex ratio (SR) and parental phenotype. We analysed offspring SR in barn swallows (Hirundo rustica) over 8 years in relation to two sexually dimorphic traits: tail length and melanin‐based ventral plumage coloration. The proportion of sons increased with maternal plumage darkness and paternal tail length, consistently with sexual dimorphism in these traits. The size of the effect of these parental traits on SR was large compared to other studies of offspring SR in birds. Barn swallows thus manipulate offspring SR to overproduce ‘sexy sons’ and potentially to mitigate the costs of intralocus sexually antagonistic selection. Interannual variation in the relationships between offspring SR and parental traits was observed which may suggest phenotypic plasticity in sex allocation and provides a proximate explanation for inconsistent results of studies of sex allocation in relation to sexual ornamentation in birds.