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.     

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.     

Immune response covaries with corticosterone plasma levels under experimentally stressful conditions in nestling barn swallows (Hirundo rustica)

Traits related to fitness are often pleiotropically linked orotherwise constrained in their expression. Organisms thereforetrade between fitness components such as number and viabilityof their offspring. The physiological mechanisms mediating suchtrade-offs, however, have been poorly investigated. We manipulatedbrood size and satiation of nestling barn swallows, Hirundorustica, to simulate the effect of two kinds of natural stresses,i.e., long-term intense competition in a large brood and acutefood deprivation, and we measured their effect on body condition,T cell–mediated immune response, and corticosterone, themain hormone mediating the adrenocortical stress-response. Broodenlargement increased corticosterone levels compared with thosefor brood reduction, and brood enlargement depressed immuneresponse, body mass, and condition. Corticosterone levels markedlyincreased after food deprivation. Immune response negativelycovaried with corticosterone levels measured after long-termstress. Hence, living in a crowded nest and with food deprivationelicited a stress response mediated by corticosterone, and depressedan important component of offspring fitness such as T cell–mediatedimmunity. The negative covariation between circulating corticosteroneand immunity suggests that the trade-off between offspring numberand quality is mediated by variation in plasma levels of corticosterone,which has immunosuppressive effects.     

Experimental manipulation of tail ornament size affects the hematocrit of male barn swallows (Hirundo rustica)

Ornamental tail feathers of male barn swallows (Hirundo rustica) confer an advantage in sexual selection because long-tailed males are preferred by females. However, the size of tail ornaments exceeds the natural selection optimum and males are predicted to pay an energetic cost for flying, directly related to tail length. An increase in hematocrit is an adaptive response to enhance oxygen uptake, for example during periods of intense locomotory activity. In this study, we analyzed the effect of experimental manipulation of tail length on the hematocrit of male barn swallows from an Italian and a Spanish population. We predicted that the natural decrease in hematocrit during the breeding season would be reduced by experimental elongation and enhanced by experimental shortening of tail ornaments. The results showed that the decrease in hematocrit was significantly different among tail treatments, and tail-elongated males had the smallest hematocrit reduction. In Italy, the hematocrit of tail-elongated males did not change after tail manipulation, while that of two control groups and tail-shortened males decreased. A comparatively high hematocrit in males with experimentally enlarged tail ornaments may be a response to increased energetic requirements and, hence, to oxygen demands for flying imposed by their tail morphology. Received: 22 June 1996 / Accepted: 23 October 1996     

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.     

Features of begging calls reveal general condition and need of food of barn swallow (Hirundo rustica) nestlings

Altricial offspring of birds solicit food provisioning by complexbegging displays, implying acoustic and visual signals. Differentcomponents of begging behavior may function as reliable signalsof offspring state and thus reproductive value, on which parentsbase optimal parental decisions about allocation of criticalresources (e.g., food). We experimentally manipulated componentsof general condition of nestling barn swallows (Hirundo rustica)by (1) altering brood size by cross-fostering an unbalanced number of nestlings between pairs of synchronous broods andthus manipulating the level of within-brood competition forfood, (2) injecting some nestlings with a harmless immunogen,simulating an infection, and (3) preventing part of the nestlingsfrom receiving food for a short period while establishing controlgroups. We recorded rate of begging response by individual nestlings as parents visited the nest and recorded begging calls usinga DAT recorder to analyze six sonagraphic features of vocalizations.Our factorial experiment revealed that nestlings deprived offood begged more frequently when parents visited the nest comparedto their non—food-deprived nest mates. Food deprivationincreased duration of syllables forming begging calls, whereas brood size enlargement resulted in increased latency of responseto parental calls. Heavy nestlings in good body condition vocalizedat a relatively low peak frequency. To our knowledge, thisis the first study in which begging rate and sonagraphic structureof begging calls are shown to reliably reveal a diverse setof components of offspring general state, on which parental decisions may be based.     

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.     

Testosterone effects on the immune system and parasite infestations in the barn swallow (Hirundo rustica): an experimental test of the immunocompetence hypothesis

The immunocompetence hypothesis predicts that testosterone (T)enhances the expression of male secondary sexual characterswhile exerting a suppressive effect on the immune system therebyexposing hosts to higher intensities of parasite infestations.In a natural population of barn swallow (Hirundo rustica) males,the intensity of infestation by some ectoparasites was negativelycorrelated with tail length and was positively correlated withimmunoglobulin levels, but no clear relationship was observedbetween immune responses (leukocyte counts, immunoglobulins)and tail length. Males implanted with T had higher intensitiesof parasite infestations at the time of recapture than controlmales, and T-implanted males experienced an increase in countsof eosinophils. In T-implanted males, immunoglobulin levelsinitially decreased and then increased as time from implantationelapsed. Among T-implanted males, those with longer tails hada smaller increase in eosinophil counts, tended to experiencea smaller increase of parasite infestations, and were more likelyto survive until the following breeding season than those withshorter tails. The relationships between parasite burden, immunesystem, and exaggeration of tail length in the natural populationof males are consistent with some aspects of the immunocompetencehandicap hypothesis. The results from the manipulation of Tplasma levels are also partly consistent with the hypothesis,since T-implantation resulted in higher levels of parasite infestations,but contradict the assumption of an obligatory immunosuppressiveeffect of T. Higher activation of the immune system of T-implantedmales indicate that high T plasma levels imposed a two-foldcost because of the effects on parasites and the immune responseto parasites, and this suggests that the effect of T on parasitesmight not be mediated by the immune system of the host. Theresults of the manipulation of T plasma levels support the handicapversion of the immunocompetence hypothesis since high quality,long-tailed males paid less in terms of activation of the immunesystem, change in parasite infestations, and chances of survivalthan low-quality, short-tailed males.     

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.     

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.     

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.     

Immune response of male barn swallows in relation to parental effort, corticosterone plasma levels, and sexual ornamentation

Life-history theory posits trade-offs between fitness components. Reproduction negatively affects physiology and immune systemfunctioning, and the effect of this form of stress may be mediatedby glucocorticosteroids. We manipulated brood size of barnswallows (Hirundo rustica) to study the effect of stress arisingfrom reproductive effort on corticosterone levels of males.We also measured T-cell—mediated immunocompetence by intradermally injecting birds with phytohemagglutinin, whichis mitogenic to T-lymphocytes. The results confirmed the predictionof a negative effect of parental effort on lymphoproliferativeresponse. We found no covariation between immune response andcorticosterone levels. Males with long tails, an ornament currentlyunder directional sexual selection, had a relatively large T-cell response to the mitogen, consistent with models of parasite-mediated sexual selection predicting higher levels of immune defensein highly ornamented males. In addition, males with large sexualornaments had relatively low corticosterone levels at the endof the parental period. These results can be reconciled withthe hypothesis proposing a trade-off between parental activitiesand adaptive immunity and suggest that highly ornamented malesare less exposed or less susceptible to stress arising fromparental effort.     

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.     

Sexual ornamentation and immunocompetence in the barn swallow

The handicap hypothesis of honest signaling suggests that secondarysexual characters reliably reflect phenotypic or genotypic qualityof signalers. This hypothesis is based on the assumptions thatsignals are costly to produce and/or maintain and the cost ofa given level of signaling is higher for low quality than forhigh quality signalers. We tested these assumptions in a fieldexperiment in which the size of a secondary sexual character[tail length in male barn swallows (Hirundo rustica)] was experimentallymanipulated. Males were randomly assigned to tail elongation,tail shortening, or two control treatments (tail manipulation,or just capture, ringing, and handling). Male barn swallowswere challenged with an injection of sheep red blood cells,and blood was sampled on the day of first capture and after3 to 4 weeks for determination of concentrations of gamma-globulins.Tail-elongated males did not increase levels of gamma-globulinswhile males of the other three groups demonstrated increases.Analyses of variation in gamma-globulins within treatment groupsrevealed a positive correlation between gamma-globulins andoriginal tail length among males with elongated tails. Theseresults suggest that tail length imposes an immu-nocompetencecost on males, and that males with naturally long tails aredifferentially better able to cope with this cost.     

The effects of temperature, altitude and latitude on the arrival and departure dates of the swallow Hirundo rustica in the Slovak Republic

The (barn) swallow Hirundo rustica is a traditional harbinger of spring in many countries of the Northern Hemisphere. This paper uses information on the arrival and departure dates of the swallow in the Slovak Republic for the 30 years 1961–1985 and 1996–2000. Records were taken at 19 locations throughout the Republic representing an altitude range from 105 m to 760 m. Monthly temperature data were constructed from six meteorological stations. With the use of regression techniques, trends towards later arrival, earlier departure and the effects of latitude, altitude and temperature are all apparent. Received: 25 October 2000 / Revised: 23 April 2001 / Accepted: 23 April 2001     

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.     

Song repertoire size varies with HVC volume and is indicative of male quality in song sparrows (Melospiza melodia)

Complex birdsong is a classic example of a sexually selected ornamental trait. In many species, females prefer males with large song repertoires, possibly because repertoire size is limited by the size of song control nuclei which reflect developmental success. We investigated whether song repertoire size was indicative of brain area and male quality in song sparrows (Melospiza melodia) by determining if repertoire size was related to the volume of song control nucleus HVC, as well as several morphological, immunological and genetic indices of quality. We found that males with large repertoires had larger HVCs and were in better body condition. They also had lower heterophil to lymphocyte ratios, indicating less physiological stress and a robust immune system as measured by the number of lymphocytes per red blood cell. Song repertoire size also tended to increase with neutral-locus genetic diversity, as assessed by mean d2, but was not related to internal relatedness. Our results suggest several mechanisms that might explain the finding of a recent study that song sparrows with large song repertoires have higher lifetime fitness.     

Rapid temporal change in frequency of infanticide in a passerine bird associated with change in population density and body condition

Sexually selected infanticide, whereby unmated males obtaina mate by killing the dependent offspring of an already matedfemale, is a common alternative reproductive strategy in manyanimals. I estimated the frequency of infanticide in a populationof barn swallows, Hirundo rustica, during the period 1977–2002.Population size decreased by more than a factor 10 during thisperiod, and this decrease was associated with an increase inmortality, selecting for adults with better body condition.Density-dependent effects acted on infanticide through the relationshipbetween the relative number of unmated males and populationsize. Because males in prime condition are better able to defendtheir nests against infanticidal males, the frequency of infanticidedecreased as mean tail length and mean body condition of malesincreased during the study period. Therefore, a rapid decreasein population size, a decrease in the abundance of unmated males,and a concomitant increase in body condition have changed theimportance of infanticide from being a major cause of mortalityaccounting for more than 25% of all nestling mortality to beingalmost completely absent during a period of 25 years.