Song and immunological condition in male barn swallows (Hirundo rustica)

Male secondary sexual characters may have evolved as intra-or intersexual signals of male phenotypic or genetic quality.In birds, singing performance may have the function to honestlyreveal health and vigor of individual males. Infectious diseasesand poor body conditions would therefore be expected to negativelyinfluence singing performance. Since bird pathogens are knownto elicit both a humoral and a cell-mediated immune response,it can be predicted that a negative relationship exists betweensinging performance and activity of the immune system. Thisprediction was tested for the first time in this correlationalstudy. The relationships between song rate and features andhematological variables (concentration of leukocytes in peripheralblood, ratio of gamma-globulins to total plasma proteins, bloodcell sedimentation rate, hematocrit) and body condition wereanalyzed in a population of bam swallows (Hirundo rustica).Song rate was negatively correlated with lymphocyte concentrationand with the ratio of gamma-globulins to plasma proteins. Spectrographicanalysis showed that features of song were not significantlycorrelated with hematological variables or body condition. Thelevel of circulating testosterone was not correlated with songrate nor hematological variables. This study is the first toshow a correlation between a bird's singing performance andhematological profile and suggests that song rate of male barnswallows may reflect their health status. Song in this speciesmight thus have evolved because it allows prospecting femalesto assess aspects of phenotypic and/or genetic quality of potentialmates     

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.     

Digit ratios, secondary sexual characters and condition in barn swallows Hirundo rustica

The second and fourth digit length ratio (2D:4D) is sexuallydimorphic in many vertebrates. This ratio has been suggestedto provide an estimate of steroid levels encountered duringprenatal development, which may have organizational consequencesfor physiology and behavior of adults. However, recent studiesshowed that the relation between digit ratio and steroids seemsinconsistent and may vary among species and populations. Wetested the hypothesis that digit ratios would be correlatedwith the expression of secondary sexual characters, using thebarn swallow (Hirundo rustica) as a model system. This was doneby testing whether variation in 2D:4D ratio was correlated withtail length and features of song, which are important secondarysexual characters positively correlated with circulating steroidconcentration in adult birds. Furthermore, we examined the predictionthat male and female digit ratios would correlate with bodymass in an antagonistic way. There was no significant sexualdimorphism in digit ratio, which may be due to low levels ofsexual selection in this population. Adult right 2D:4D ratiowas negatively linked to tail length but not to male song output.Moreover, right 2D:4D ratio was negatively correlated with bodymass in male and positively in females. These results are consistentwith high digit ratios reflecting low levels of testosteronein this bird species.     

The function of long tails in female barn swallows (Hirundo rustica): an experimental study

The outermost tail feathers in male barn swallows (Hirundo rustica)are the target of a strong directional female mate preference.The tail ornament is also expressed in females, since femaleshave considerably longer tails than juveniles, either due to(1) a strong genetic correlation between the characters in thetwo sexes, or (2) direct sexual selection on females. To discriminatebetween these two hypotheses, we manipulated the length of theoutermost tail feathers in female barn swallows shortly afterarrival by either shortening or elongating the outermost tailfeathers, or maintaining their length among control individuals.Start of laying of the first clutch, reproductive performance,or provisioning of offspring did not show any significant differencesamong treatments. Original female tail length before manipulationwas unrelated to reproductive performance, while male tail lengthexplained some variation in the number of clutches and, to someextent, the total number of eggs laid per year. Females withlonger tails arrived earlier at the breeding grounds. Manipulatedfemale tail length was positively correlated to the tail lengthof their mates. Our results support the correlated responsehypothesis but do not support the sexual selection explanationfor the existence of exaggerated tail feathers in female barnswallows.     

Haemosporidian parasites depress breeding success and plumage coloration in female barn swallows Hirundo rustica

Parasites are major effectors of natural selection and also play a role in sexual selection processes. Haemosporidian blood parasites are common in vertebrates and have been shown to vary in their effects depending on both the parasite and host species, on the host trait investigated as well as on host condition and stage of infection. Here we investigated infection of adult barn swallows Hirundo rustica by Plasmodium, Leucocytozoon and Haemoproteus species during the chronic stage of infection and the consequences for host fitness traits. Prevalence was higher than 10% only for Plasmodium. Chronic stage infection by Plasmodium was associated with reduced female breeding success, but did not affect breeding dates. Infection did not affect the expression of male secondary sexual traits (tail length and melanin‐based plumage coloration), but was associated with paler coloration of females. Finally, we found a negative effect of infection by Plasmodium on feather growth rate in older but not in yearling individuals. Because feathers are moulted during wintering in sub‐Saharan Africa where infection of barn swallows by Plasmodium occurs, our results suggest that male secondary sexual traits have little potential to reveal acute‐stage infection whereas plumage coloration of females may advertise their infection status. In addition, these results suggest that infection by Plasmodium can influence the course of plumage moult. Thus, our results add to the observations of negative effects of haemosporidian infection on fitness traits in birds and provides evidence that these effects can vary among traits and in relation to age and sex.     

Impaired swimming behaviour and morphology of sperm from barn swallows Hirundo rustica in Chernobyl

We investigated the motility and morphology of live sperm from barn swallows Hirundo rustica breeding in radioactively contaminated areas around Chernobyl and control areas in Ukraine in order to test the hypothesis that swimming behaviour and morphology of sperm was impaired by radioactive contamination. We obtained sperm samples from 98% of sampled birds, thus avoiding sampling bias due to the fraction of males not producing sperm samples. Analyses of within- and between-sample repeatability revealed significant and intermediate to large estimates for all sperm parameters. There were significant differences between the Chernobyl area and the control area for two of 11 sperm behaviour parameters, and significant interactions between area and year for six of these parameters. The proportion of sperm with abnormal morphology was elevated in barn swallows from Chernobyl. A principal component (PC) analysis revealed four significant axes that explained 88% of the variance in sperm behaviour parameters. One of these principal components differed between areas, and three components showed significant year by area interactions. PC2 representing the frequency of slow sperm increased with increasing radiation in one year, but not another. PC3 representing sperm with high linearity, small amplitude of lateral head displacement and low track velocity decreased with increasing background radiation level. PC4 reflecting a large proportion of static sperm with high beat cross frequency increased with increasing background radiation level. Sperm behaviour as reflected by principal components was predictable among years from information on level of radiation, and it was predictable among sites in different years. These results are consistent with the hypothesis that sperm behaviour and morphology have been affected by radiation due to the Chernobyl accident.     

DNA fingerprinting reveals relation between tail ornaments and cuckoldry in barn swallows, Hirundo rustica

In an experimental study in Denmark, it was previously foundthat male barn swallows (Hirundo rustica) with elongated tailstreamers obtained an apparent fitness advantage through earlierpairing, an increased frequency of second clutches, and highertotal reproductive success per season. In a parallel study offive barn swallow colonies in Ontario, Canada, we also foundthat elongated males paired earlier and thus were apparentlypreferred by females. Now, using DNA fingerprinting on familiesfrom two of those Ontario colonies, we show that five elongatedmales fathered only 59% of the offspring in their nests, whereassix shortened males fathered 96% of their nestlings. Thus, althoughelongated males were clearly preferred by females at the timeof pair formation, tail elongation may have hampered the abilityof a male to guard his mate, resulting in an increase in extrapairfertilizations (EPFs). A significant negative correlation betweenthe number of EPFs and natural tail length in this experimentalstudy also suggests that tail streamer length may reflect malequality. (Behav Ecol 1990; 2: 90–98)     

First observation of African tigerfish Hydrocynus vittatus predating on barn swallows Hirundo rustica in flight

A population of African tigerfish Hydrocynus vittatus from the Schroda Dam, actively prey on barn swallows Hirundo rustica in flight. This behaviour was discovered during a radio telemetry study and documented using a motion picture video camera. These results show that an avivorous diet is a part of the feeding biology of H. vittatus, and may occur in other populations.     

Behavioural and energetic responses to body state in male and female barn swallows (Hirundo rustica)

Females and males often have different roles when attending young. The factors responsible for shifts in the balance of effort when both sexes provision their young are not clear. This study asked if sex-specific behaviour and provisioning rules in barn swallows (Hirundo rustica) were dependent on individual body-state or affected by the state of their provisioning partner. To assess this male and female barn swallows underwent overnight warming manipulations whilst provisioning 10-14 day old nestlings, a time when energetic demands are maximal. The overnight warming treatment reduced thermoregulatory costs and provided birds with extra energy reserves at dawn. Only one member of a pair was manipulated in this way, whilst their partners were left un-manipulated to assess their response to their partner's elevated body-state. The energetic and behavioural responses to these manipulations were followed over the subsequent 24-h. I found that warmed male and female barn swallows increased their energy expenditure and nest visitation rates to the same extent after manipulation, implying a trade-off in resource allocation, which was biased towards reproductive effort. There was no effect of gender. Males paired with manipulated females showed no energetic or behavioural adjustments, however, females paired with manipulated males tended to increase both energy expenditure and nest visitation. This study provides evidence that energy reserves constrain behaviour, and that male and female swallows normally follow the same state-dependent rules when provisioning young.     

Ecological barriers shaping fuel stores in barn swallows Hirundo rustica following the central and western Mediterranean flyways

The crossing of ecological barriers is among the most energy-demanding and risky phases of migration. Scanty field data exist on the relationships between ecological barriers and pre-migratory fuel storing in songbirds. The aim of this study was to analyse whether the distance to be covered across ecological barriers can be considered as a factor affecting pre-migratory fuel stores in barn swallows Hirundo rustica following the two main western European flyways, funnelling through Iberia and Italy. Data refer to 13029 swallows and were collected during July–October in 1997–1998 at 19 roost sites, scattered over Spain and Italy (south of 43°N). During the post-breeding phase (PB, July–August) energy stores did not differ significantly between the two geographical areas, whereas during the pre-migratory phase (PM, September–October) swallows in Italy carried larger energy stores than those in Spain. Assuming that swallows leave for migration from the fuelling site, we found a significant positive correlation between the width of ecological barriers and an average index of energy stores for each roost site during the PM phase. The width of ecological barriers (along a N-S migration route) was expressed as (1) the distance between the roost site and the coast of North Africa (representing the Mediterranean Sea), and (2) the distance between the roost site and the southern margin of the Sahara desert (the total width of ecological barriers). The weaker correlations obtained when considering only the Mediterranean as a barrier suggest that swallows may cross the desert without substantial refuelling in North Africa. Hence, we showed that fuel stores have a degree of population-specific variability among Italian and Iberian barn swallows and that the extension of ecological barriers may play a role in determining the amount of stores needed for the migratory flight.     

The maintenance of phenotypic divergence through sexual selection: An experimental study in barn swallows Hirundo rustica

Previous studies have shown that sexual signals can rapidly diverge among closely related species. However, we lack experimental studies to demonstrate that differences in trait‐associated reproductive performance maintain sexual trait differences between closely related populations, in support for a role of sexual selection in speciation. Populations of Northern Hemisphere distributed barn swallows Hirundo rustica are closely related, yet differ in two plumage‐based traits: ventral color and length of the outermost tail feathers (streamers). Here we provide experimental evidence that manipulations of these traits result in different reproductive consequences in two subspecies of barn swallow: (H. r. erythrogaster in North America and H. r. transitiva in the East Mediterranean). Experimental results in Colorado, USA, demonstrate that males with (1) darkened ventral coloration and (2) shortened streamers gained paternity between two successive reproductive bouts. In contrast, exaggeration of both traits improved reproductive performance within H. r. transitiva in Israel: males with a combination treatment of darkened ventral coloration and elongated streamers gained paternity between two successive reproductive bouts. Collectively, these experimental results fill an important gap in our understanding for how divergent sexual selection maintains phenotype differentiation in closely related populations, an important aspect of the speciation process.     

Aerodynamic costs of long tails in male barn swallows Hirundo rustica and the evolution of sexual size dimorphism

Exaggerated tail feathers of birds constitute a standard exampleof evolution of extravagant characters due to sexual selection.Such secondary sexual traits are assumed to be costly to produceand maintain, and they usually are accompanied by morphologicaladaptations that tend to reduce their costs. The aerodynamiccosts for male barn swallows Hirundo rustica of having longtails were quantified using aerodynamics theory applied to morphologicaldata from seven European populations. Latitudinal differencesin tail length were positively correlated with differences inflight costs predicted by aerodynamics theory. A positive relationshipbetween aerodynamic costs of long tails and the degree of sexualsize dimorphism was found among populations. Latitudinal differencesin foraging costs may result in tail length being relativelysimilar in males and females in southern populations, whereasthe low foraging costs for males in northern populations mayallow them to cope with higher aerodynamic costs, giving riseto large sexual size dimorphism. Enlargement of wingspan inmales can alleviate but not eliminate the costs of tail exaggeration,and therefore differences in aerodynamic costs of male ornamentswere maintained among populations. Sexual size dimorphism in thebarn swallow arises as a consequence of latitudinal differencesin the advantages of sexual selection for males and the costsof long tails for males and females.     

Cost of reproduction, T-lymphocyte mediated immunocompetence and health status in female and nestling barn swallows Hirundo rustica

We investigate the trade-off between reproductive effort, health status and T-lymphocyte acquired immunity in female and nestling barn swallows Hirundo rustica using a brood size manipulation experiment. Maternal and total feeding effort increased with experimental brood size. Parents did not fully compensate for the increased food demand of the enlarged broods and as a consequence the per capita feeding rate of nestlings decreased with increasing experimental brood size. Body mass and a measure of T-cell mediated immunity in 12 days old nestlings also decreased with increasing experimental brood size. Different leucocyte concentrations and the heterophile/lymphocyte ratio – an index of stress – of nestlings did not change in relation to experimental brood size, suggesting that within brood competition did not affect stress to nestlings. The brood size manipulation had a significant effect on maternal T-cell mediated immunity, measured by the phytohemagglutinin skin test, but not on maternal body mass, haematocrit or differential or total white blood cell counts. Our results seem to support the prediction that under mild work stress females respond first by reducing the energetically expensive acquired immunity. Different leucocyte types and the heterophile/lymphocyte ratio appear less sensitive to parental workload.     

Effects of experimental tail shortening on the phenotypic condition of barn swallows Hirundo rustica: implications for tail‐length evolution

Some studies have suggested that tail streamers in the barn swallow Hirundo rustica may have been elongated 10–12 mm by sexual selection, but according to other studies, the length of these feathers is at the aerodynamic optimum or very close to it. To shed light on this issue, outermost tail feathers were experimentally shortened in male and female barn swallows by 1, 11 or 21 mm. Changes in four physiological parameters commonly used to estimate phenotypic condition in birds (weight, erythrocyte sedimentation rate, blood leukocyte concentration and heterophil/lymphocyte ratio) were checked one month later. Health improved (blood leukocyte concentration decreased) in the group of birds with tails shortened by 11 mm (both males and females), but body condition deteriorated (weight decreased) compared to the other two experimental groups. There was no significant effect of tail‐length manipulation on the other two physiological parameters. These contradictory results suggest trade‐offs between components of phenotypic condition. Possible negative relationships between condition‐related traits imply that using one or very few physiological parameters to estimate phenotypic condition might not be appropriate. The most plausible explanation for the turning point in phenotypic condition when streamers were shortened by 11 mm is that these feathers are 7–15 mm longer than the aerodynamic optimum in both sexes. Therefore, our results are consistent with the hypothesis that tail streamers have been elongated 10–12 mm by sexual selection. This conclusion disagrees with a previous study on the effect of experimental tail shortening on haematocrit, but the complexity of interpreting changes in haematocrit might account for this discrepancy.     

A comparative study of insect abundance and reproductive success of barn swallows Hirundo rustica in two urban habitats

Few studies have quantified the relative reproductive success of passerines in urban habitats. I studied food availability and reproductive success of barn swallows Hirundo rustica in two urban habitats during 2012–2015. Barn swallows breeding in the town center experienced lower insect densities than those in the town periphery. Lower food availability resulted in reduced feeding rates per capita, lower nestling body mass, longer nestling periods, longer inter‐clutch intervals, fewer first and second brood fledglings and a lower total number of fledglings produced during the breeding season in comparison to barn swallows breeding in the town periphery. I hypothesize that the lower intra‐specific competition for nest sites and fitness advantages linked to the solitary breeding in urban habitats balanced the apparent costs of reproduction in more urbanized habitats.     

Timing of migration and residence areas during the non‐breeding period of barn swallows Hirundo rustica in relation to sex and population

We investigated sex‐ and year‐dependent variation in the temporal and spatial movement pattern of barn swallows Hirundo rustica during the non‐breeding period. Hundred and three individuals equipped with miniaturized light‐level geolocators at three different breeding areas in southern Switzerland and northern Italy provided data for the analysis. We identified a region 1000 km in radius centred in Cameroon as the main non‐breeding residence area of these three geographical populations. Five residence areas of males only were in southern Africa, south of 19°S. Most individuals occupied a single site during their stay south of the Sahara. The timing of migration broadly overlapped between sexes and all geographical breeding populations. Between the two study years there was a distinct difference of 5 to 10 d in departure dates from and arrival at the breeding sites. Remarkably, the period of residence in sub‐Saharan Africa was very similar (157 d) in the two study years, but their positions in the first year (2010–2011) were about 400 km more to the north than in the second (2011–2012). Independent of the year, individuals with sub‐Saharan residence areas further north and east had a shorter pre‐breeding migration and arrived earlier than those staying further south and west. In addition, birds breeding in southern Switzerland arrived at their breeding colony 7–10 d later than those breeding only 100 km south, in the Po river plain. Our study provides new information on the variance in migration phenology and the distribution of residence areas in sub‐Saharan Africa in relation to sex, population and year. It supports the usefulness of light‐level geolocators for the study of annual routines of large samples of small birds.     

Corticosterone secretion patterns prior to spring and autumn migration differ in free-living barn swallows (Hirundo rustica L.)

Recent studies of long-distance migratory birds show that behavioural and physiological changes associated with predictable or unpredictable challenges during the annual cycle are distinctively regulated by hormones. Corticosterone is the primary energy regulating hormone in birds. Corticosterone levels are elevated during stresses but they are also modulated seasonally according to environmental conditions and life-history demands. We measured the baseline and stress-induced levels of corticosterone in the barn swallow (Hirundo rustica L.) just before spring and autumn migrations in South Africa and Finland, respectively. Barn swallows completing their pre-breeding moult had low body condition (residual body mass) and high baseline corticosterone levels in the wintering grounds. In contrast, baseline corticosterone levels in Finland were low and not related to residual mass. These data contradict the first prediction of the migration modulation hypothesis (MMH) by showing no association with baseline corticosterone levels and pre-migratory fuelling. Yet, the adrenocortical response to the capture and handling stress was notably blunted in South Africa compared to a strong response in Finland. Further, individuals that had started fuelling in Finland showed a reduced response to the handling stress. Taken together, elevated baseline corticosterone levels and high residual mass may blunt the adrenocortical response in long-distance migrants and aerial feeders such as the barn swallow. This observation lends support to the second prediction of the MMH.     

Experimental manipulation of tail length in female barn swallows (Hirundo rustica) affects their future reproductive success

Previous studies have shown no significant effect of experimentaltail length manipulation in female barn swallows (Hirundo rustica)at the beginning of a breeding season on reproductive successor behavior during that breeding season. In the present study,we investigate if tail length manipulation had any effect onreproductive performance the following year, the so-called long-termeffect, in contrast to the short-term effects already studied.We found that females with experimentally elongated externaltail feathers at the beginning of a breeding season producedless offspring during the breeding season the following yearthan did females with shortened or unmanipulated tails. Theseresults suggest that tail elongation caused flight deficienciesthat deteriorated the condition of females and eventually reducedreproductive success. The finding of long-term effects but nosignificant short-term effects for female tail elongation suggeststhat female barn swallows have the ability to adjust immediateparental investment. Detrimental effects of long tails in femalesin terms of decreased reproductive success might explain whyfemale tails are not as long as those of males. Finally, femalesmated to long-tailed (sexually attractive) males decreased theirreproductive success the following year more than did femalesmated to short-tailed males, possibly owing to differentialparental effort causing a deterioration of their condition.     

Immunoglobulin plasma concentration in relation to egg laying and mate ornamentation of female barn swallows (Hirundo rustica)

In vertebrates, offspring have a relatively inefficient immune system soon after birth. Female birds transmit immunoglobulins to the egg, which can confer protection against parasites to their offspring after hatching, but allocation of immune factors can depend on the reproductive value of the offspring as affected, for example, by the quality of their father. We analyse the variation in immunoglobulin levels of female barn swallows (Hirundo rustica) during the breeding cycle in relation to the expression of a secondary sexual character of their mates. Circulating immunoglobulins peaked on approximately the day before that of laying of their first egg, but postlaying concentration was similar to the concentration well before laying. Immunoglobulin levels per unit volume of plasma were lower for females breeding late compared with those breeding early. Haematocrit of females reached an absolute minimum on the day of laying of the third egg. In males, concentration of immunoglobulins relative to other plasma proteins did not change in relation to the breeding stage. Smaller relative concentrations of immunoglobulins and haematocrit were observed in males breeding late in the season. Immunoglobulin concentration of females was positively correlated with the level of ornamentation of their mates. These results suggest that females alter their immune profile to transmit humoral factors providing immune defence against pathogens to their offspring after hatching. This enhancement of immune protection is larger when the offsprings are of relatively large reproductive value as when sired by high quality males. Alternatively, females with relatively large immunoglobulin concentration preferentially mate with the most ornamented males.     

Viability and expression of sexual ornaments in the barn swallow Hirundo rustica: a meta‐analysis

Sexual selection results in the evolution of exaggerated secondary sexual characters that can entail a viability cost. However, in species where sexual ornaments honestly reflect individual quality, the viability cost of secondary sexual characters may be overwhelmed by variation in individual quality, leading to expect that individuals with the largest secondary sexual characters show higher, rather than lower viability. Here, we used meta‐analyses to test whether such expected positive relationship between sexual ornamentation and viability exists in the barn swallow Hirundo rustica, which is one of the most studied model species of sexual selection under field conditions. We found a mean positive effect size of viability in relation to the expression of secondary sexual characters of 0.181 (CI: 0.084–0.278), indicating that in this species the more ornamented individuals are more viable, and therefore of high quality. Analyses of moderator variables showed similar effects in males and females, the H. r. rustica subspecies rather than others and tail length rather than other secondary sexual characters. Future research emphasis on other subspecies than the European one and secondary sexual characters than tail length may help identify the sources of heterogeneity in effect sizes.