Determinants of the Mating Success of Polyterritorial Pied Flycatcher Males

Much attention has been paid to the polyterritorial mating system of some passerine birds. Here we report how a male's mating success is related to the behavioral traits of polyterritorial pied flycatcher (Ficedula hypoleuca) males. We found no evidence that the timing of polyterritoriality in relation to egg laying in the primary nest or the singing behavior of males have any influence on mating success. However, results show clearly that male mating success was improved with an increase in the distance between territories up to a distance of about 200–300 m whereupon there was no further enhancement of mating success. This finding is crucial for both the deception hypothesis and female-female aggression hypothesis which have been put forward to explain polyterritorial polygyny. Males who establish a distant second territory seemed to allocate more time to singing there. The association, although weak, between singing activity and distance between territories makes it more difficult for females to use song rate as a cue to discriminate males with a secondary territory far from the primary territory, and these are the males that are least likely to feed the young of a second female. Males who established a second territory late in relation to egg laying in the primary nest did not take over a close second territory as might be predicted from female-female aggression hypothesis.     

More colourful eggs induce a higher relative paternal investment in the pied flycatcher Ficedula hypoleuca: a cross-fostering experiment

The signalling hypothesis of eggshell colouration in birds posits that females of species with blue-green eggs signal their phenotypic quality or the quality of their eggs to their mates through deposition of the antioxidant biliverdin as pigment. Males respond by investing more in the offspring. Through a cross-fostering experiment where we have exchanged whole clutches between pairs of pied flycatcher Ficedula hypoleuca nests, we managed to break potential associations between female quality and clutch chromaticity. We show that males respond to incubated clutches with more variable and higher peak values in blue-green chroma through a higher proportional investment in nestling provisioning on day 4 of the nestling period, when males invest more heavily than females in provisioning. More variable clutches show higher peak chroma values. We also show that egg colour during the two-week incubation period has a significant effect, which is not found for the colour of eggs during the laying period. Finally, the proportion of male provisioning visits affects negatively female brooding effort and nestling mortality, and thereby has positive effects on female fitness. Blue-green chroma in the pied flycatcher functions as a signal of female or clutch quality to males which respond by adjusting their relative investment with respect to total pair effort.     

Song similarity predicts hybridization in flycatchers

Given that population divergence in sexual signals is an important prerequisite for reproductive isolation, a key prediction is that cases of signal convergence should lead to hybridization. However, empirical studies that quantitatively demonstrate links between phenotypic characters of individuals and their likelihood to hybridize are rare. Here we show that song convergence between sympatric pied (Ficedula hypoleuca) and collared flycatchers (F. albicollis) influence social and sexual interactions between the two species. In sympatry, the majority of male pied flycatchers (65%) include various parts of collared flycatcher song in their song repertoire (but not vice versa). Playback experiments on male interactions demonstrate that male collared flycatchers respond similarly to this 'mixed' song as to conspecific song. Long-term data on pairing patterns show that males singing a converged song attract females of the other species: female collared flycatchers only pair with male pied flycatchers if the males sing the mixed song type. From the perspective of a male pied flycatcher, singing a mixed song type is associated with 30% likelihood of hybridization. This result, combined with our estimates of the frequency of mixed singers, accurately predicts the observed occurrence of hybridization among male pied flycatchers in our study populations (20.45% of 484 pairs; predicted 19.5%). Our results support the suggestion that song functions as the most important prezygotic isolation mechanism in many birds.     

Polygyny in the pied flycatcher,Ficedula hypoleuca: a test of the deception hypothesis

The deception hypothesis has been proposed as an explanation for polygyny in the pied flycatcher. According to this hypothesis, already-mated males hide their mating status with polyterritorial behaviour and thereby increase their chances of obtaining a second mate. In a study area at Oslo, Norway, secondary females raised 84% as many fledglings as did concurrent monogamous and primary females. The unmated males sang most of the time near their nest site, whereas the already-mated males frequently disrupted singing for longer periods in their secondary territories to visit their primary nest; such visits to the primary nest occurred both before and after the time of their second mating. The behaviour of the males suggests that deception of females is not an evolutionarily stable strategy, as an observant female would soon discern the male's status. Another difficulty with the deception hypothesis is that secondary females laid larger clutches than primary females. The number of young fledged from secondary nests was not dependent on the distance to the primary nest. The deception hypothesis was not supported by the data, and the reduced reproductive success of secondary females may be explained by the cost of searching for a mate.     

Early arrival is not associated with more extra‐pair fertilizations in a long‐distance migratory bird

When assessing the benefits of early arrival date of migratory birds, a hidden and often ignored component of males’ fitness is the higher chance of early‐arriving birds to obtain extra‐pair fertilizations. Here we investigated how extra‐pair paternity might affect the relationship between male arrival date and number of fertilizations in a model study system, the European pied flycatcher Ficedula hypoleuca. For this purpose, we sampled and genotyped breeding pairs, unpaired males and offspring (including embryos from unhatched eggs when possible) of a Dutch pied flycatcher population. Detailed information on arrival date of males, egg laying date of their social mates and nest success was also recorded. Early‐arriving males had early‐laying females and males with early‐laying females had a higher probability of siring extra‐pair eggs and obtain more fertilizations. However, male arrival date alone did not correlate with the probability to gain extra‐pair paternity and neither to the amount of fertilized eggs. Both early‐ and late‐arriving males had a higher probability of losing paternity in their own nest compared to birds with an intermediate arrival date. Finally, late‐arriving males were more likely to remain unpaired but, interestingly, a few of these birds obtained paternity via extra‐pair copulations. Because earlier arrival date did not lead to more extra‐pair fertilizations and because such relationship seems to be driven mainly by the female's laying date, we conclude that the contribution of extra‐pair paternity to the overall fitness benefits of early male arrival date is relatively small.     

Phenomenon of visiting in the pied flycatcher (Ficedula Hypoleuca Pall., Passeriformes, Aves) in the breeding period

Strange visitors to the pied flycatcher nest-boxes during the brood-rearing period were investigated in the Moscow oblast during 15 seasons. The total amount of visits was 760. Most of the visits (94%) were made by males and 5% and 1% were made by females and young birds with juvenile plumage, respectively. Both bachelor and paired males of various ages were among the visitors. Most of the adult birds and all young ones behaved as ??inspectors??; a part of the visitors tried to feed nestlings. Among them, only nine males and a female were constant ??helpers.??     

Effects of long-acting testosterone treatment on freeliving pied flycatchers, Ficedula hypoleuca, during the breeding period

Breeding behaviour and spermatogenesis of all males in a population of pied flycatchers, Ficedula hypoleuca, were experimentally prolonged by long-acting testosterone. The behaviour of these birds was compared with that of birds from an untreated population and a population where the males were given the vehicle only. The testosterone treatment prolonged territorial behaviour, and a higher percentage of nests without a feeding male during the nestling period was found in the experimental area. The proportion of polygamous males did not however differ between the experimental and control areas. The feeding activity of those testosterone-treated males returning to their home territories was markedly depressed. The female of such a pair did not compensate for the male's low feeding activity, but fed the nestlings as she would have done with a normal untreated male at the nest. On the other hand, females without a male present during the nestling period compensated for their mates' absence by increasing their own feeding frequency. It was also shown that the song of the male pied flycatcher is dependent upon androgens. The testosterone-treated males produced fewer fledglings than the control males.     

Sexual differences in moult–breeding overlap and female reproductive costs in pied flycatchers, Ficedula hypoleuca

1. In this study I show that a sexual difference in timing of the post-nuptial moult frequently occurs in a sub-arctic population of the pied flycatcher.
2. Most pairs started to moult after fledging of their young, but an overlap between moult and nestling feeding was more common among males than females. This sexual difference in moult–breeding overlap increased as the season progressed.
3. Females with moult–breeding overlap laid smaller clutches than non-moulting females. In addition to many other factors explaining the seasonal decline in clutch size that has been found for many bird species, it is possible that females adjust their clutch size according to their own risk of having to start moulting while still feeding the nestlings.
4. Nearly 24% of the females were deserted by their mate before the young fledged. Desertion imposed no fitness costs to males in terms of fledgling number or quality, suggesting that their females managed to adjust their care for the loss of male care.
5. Deserted females started moulting later than aided females, which may be a result of their increased reproductive investment.
6. Deserted females and females aided by moulting males had lower survival rate than females aided by non-moulting males.
7. These findings suggests that delayed moult may be one mechanism causing inter-annual reproductive costs in birds, and the relationship between a sexual difference in timing of moult and its fitness consequences may be widespread among passerine birds.     

Heterospecific female mimicry in Ficedula flycatchers

Mimicry is a widespread phenomenon. Vertebrate visual mimicry often operates in an intraspecific sexual context, with some males resembling conspecific females. Pied flycatcher (Ficedula hypoleuca) dorsal plumage varies from the ancestral black to female‐like brown. Experimental studies have shown that conspecific and heterospecific (collared flycatcher, F. albicollis) individuals of both sexes respond, at least initially, to brown individuals as if they were female. We quantified the perceptual and biochemical differences between brown feathers and found that brown pied flycatcher males are indistinguishable from heterospecific, but not from conspecific, females in both aspects. To our knowledge, this is the first evidence of a visual mimetic signalling system in a sexual context where the model is heterospecific to the mimic. By only mimicking heterospecific females, brown pied flycatcher males can establish territories next to the more dominant collared flycatcher in sympatry, suffer less aggression by darker conspecifics in allopatry and preserve within‐species sexual recognition throughout the breeding range. A closer look at the evolutionary history and ecology of these two species illustrates how such a mimetic system can evolve. Although likely rare, this phenomenon might not be unique to Ficedula flycatchers.     

Black-and-white plumage in male pied flycatchers (Ficedula hypoleuca) reduces the risk of predation from sparrowhawks (Accipiter nisus) during the breeding season

Bright colors in birds might signal that they are undesirableas prey (aposematic), an idea that has been difficult to test.When stuffed pied flycatchers Ficedula hypoleuca are exposedto migrating sparrowhawks Accipiter nisus in spring or in autumn,the hawks attack cryptic females more often than bright males.To achieve better statistical control and to assess whethermale plumage also reduces predation risk in the breeding seasonand in the nesting habitat of the pied flycatcher, I placedpairs of male and female flycatcher mounts in similar positionsnear 22 nests of sparrowhawks. The hawks attacked mainly femalemounts, verifying that the preference is real. The sparrowhawkscaught at least 19 live pied flycatchers; 12 young, 5 adultmales, 1 adult female, and 1 female or young. Hawks that caughtan adult male seemed to prefer attacking female mounts. I discussthree interpretations of these results, suggesting that black-and-whitemale flycatchers may benefit from being a novel and aberrantprey, at least early in the breeding season.     

Experimental evidence that egg color indicates female condition at laying in a songbird

The signaling hypothesis of eggshell coloration in birds isbased on the assumption that females of species with blue-greeneggs signal their phenotypic quality to their mates throughdeposition of the antioxidant biliverdin as pigment. Egg pigmentationmay be an expression of the condition of females at laying orof genetic linkages between egg color and female performancevariables. We have supplemented 16 pied flycatcher, Ficedulahypoleuca, females with mealworms before and during laying andcompared the mass and color of their eggs as measured on theday of laying to those of 16 control females with the same nestconstruction and laying dates and clutch sizes. Supplementedfemales laid significantly heavier and more intensely blue-greeneggs than control females. Egg blue-green chroma was significantlyassociated with the amount of biliverdin in eggshells. Egg color,and thus biliverdin content, is an expression of female conditionat laying.     

Male polyterritoriality and imperfect female choice in the pied flycatcher, Ficedula hypoleuca

Polyterritoriality, the occupation of two spatially separateterritories by male birds, has been suggested to enable malesto conceal their pairing status. The idea that males deceivefemales has recently been questioned with arguments that femaleswould easily be able to detect polyterritorial males and thatthey mate in the second territories because better breedingoptions are not available close by. We arranged for pied flycatcher(ficedula hypoleuca) females a choice between neighboring unmatedand already-mated males. Females were unable to discriminateagainst already-mated males, even though their breeding successthereby would have been increased. These results allow rejectionof any polygyny models that assume females use male pairingstatus as a criterion for mate choice. Females would reducethe probability of mating polygynously by choosing dull, yearlingmales with high song rate, even though in most cases it is difficultto differentiate already-mated and unmated males. In fact, femalesdid not prefer colorful males, opposing a general pattern foundin other bird species. However, females did not specificallyprefer dull males nor did they respond to slight differencesin song rates. The seemingly nonadaptive, imperfect female behaviorsuggests that the evolution of female selectivity is constrained,allowing deception by males to be successful in the evolutionary‘arms race’ between the sexes. [Behav Ecol 1990,-1:171–177]     

Egg colour reflects the amount of yolk maternal antibodies and fledging success in a songbird

Blue-green colours in avian eggs have been proposed as post-mating signals of female phenotypic quality to their mates. Egg colour may not only indicate female value, but also the quality of the eggs themselves and of resulting offspring. To date, there has been no demonstration of an association between egg colour and egg or offspring immune quality. We here show that the intensity of blue-green colour of pied flycatcher Ficedula hypoleuca eggs reflects the amount of maternal antibodies in the yolk, a form of passive immunity crucial for offspring performance. Moreover, egg colour predicts fledging success. Also, incubating females in better condition lay more colourful eggs. The immunoglobulin level in incubating females is positively associated with that in the eggs. These results support the signalling hypothesis of eggshell coloration, underlining its role as an indicator of trans-generational transmission of immune defences in birds.     

Individual color variation and male quality in pied flycatchers (Ficedula hypoleuca): a role of ultraviolet reflectance

Bright coloration of males in many animal species has inspiredresearchers for more than a century. In this field study, weinvestigated whether color variation between individuals isrelated to individual quality in pied flycatcher (Ficedulahypoleuca) males in terms of arrival time at the breeding sites.In addition to traditional visual color scoring, plumage color was measured using spectroradiometric measurements between 320and 700 nm. This range includes the near-ultraviolet wavebandfrom 320 to 400 nm. Males that arrived earlier at breedingsites had higher proportional UV reflectance in the crown andmantle. The proportional UV reflectance in the crown and mantlewas not related to traditionally scored general brownness inmales. However, adult males had a higher proportion of ultravioletin the plumage than yearling males or females. These resultssuggest that in pied flycatcher males, the UV reflectance ofplumage may be positively correlated with individual quality.     

Arrival and onset of breeding of three passerine birds in eastern Finland tracks climatic variation and phenology of insects

Anthropogenic climate change poses a challenge to the annual cycles of migratory birds. It has become urgent to understand whether migratory birds are able to advance their spring phenology when the climate is warming and whether they are able to adjust these phenological phases to the spring phenology in their breeding areas. In this work, we studied long‐term trends in first arrival and onset of breeding for three passerine birds in eastern Finland; the pied flycatcher Ficedula hypoleuca, the common redstart Phoenicurus phoenicurus and the great tit Parus major. The pied flycatcher and the common redstart are long‐distance migrants while the great tit is a partial migrant in Finland. We asked what environmental variables best explain the first arrival or onset of breeding, if there is evidence of ‘thermal delay’ (long‐term increase in the accumulated temperatures) at arrival or onset of breeding and if the interannual variation in the onset of breeding correlates with variation in spring phenology of local insects. We found that the pied flycatcher and the common redstart had advanced their first arrival (explained by increased temperatures at the migration route), but we found no long‐term change in the onset of breeding (explained by local temperatures). Also, the onset of breeding of the great tit is tracking local temperatures. We found no or only weak evidence of thermal delay at arrival or onset of breeding for any of the species. The onsets of breeding for the pied flycatcher and the great tit are also closely tracking the spring phenology of the local insects. The stable or increasing population sizes of all three species in Finland could be a result from their ability to effectively track climatic and environmental variation.     

The effects of sex, age and breeding success on breeding dispersal of pied flycatchers along a pollution gradient

We modelled breeding dispersal of an insectivorous bird, the pied flycatcher (Ficedula hypoleuca) around a point source of heavy metals (a copper smelter). We tested for the effects of sex, age, breeding success and environmental pollution on breeding dispersal distances of F. hypoleuca females and males. Unlike many earlier studies on breeding dispersal, we took into account distance-dependent sampling bias by including in our model the recapture probabilities at different distances from the site of origin. Our results show that F. hypoleuca females disperse much farther (on average 7.9 km) from their breeding sites than what was previously thought. In contrast, males only disperse short distances (on average 190 m). Breeding success affected female breeding dispersal distances depending on female age: young females moved on average 8 km from their previous breeding place irrespective of their breeding success, while old females only seemed to move this far when their fledgling production was good. Females successful in their breeding dispersed as far as less successful females, or, among old birds, even farther. Females which dispersed long distances produced more fledglings after the movement than those staying near their previous breeding site. Degree of environmental pollution had no effect on female or male breeding dispersal distances. A polluted and unproductive environment does not seem to stimulate F. hypoleuca parents to move to more profitable territories.     

Sympatric divergence and clinal variation in multiple coloration traits of Ficedula flycatchers

Geographic variation in phenotypes plays a key role in fundamental evolutionary processes such as local adaptation, population differentiation and speciation, but the selective forces behind it are rarely known. We found support for the hypothesis that geographic variation in plumage traits of the pied flycatcher Ficedula hypoleuca is explained by character displacement with the collared flycatcher Ficedula albicollis in the contact zone. The plumage traits of the pied flycatcher differed strongly from the more conspicuous collared flycatcher in a sympatric area but increased in conspicuousness with increasing distance to there. Phenotypic differentiation (P_ST) was higher than that in neutral genetic markers (F_ST), and the effect of geographic distance remained when statistically controlling for neutral genetic differentiation. This suggests that a cline created by character displacement and gene flow explains phenotypic variation across the distribution of this species. The different plumage traits of the pied flycatcher are strongly to moderately correlated, indicating that they evolve non‐independently from each other. The flycatchers provide an example of plumage patterns diverging in two species that differ in several aspects of appearance. The divergence in sympatry and convergence in allopatry in these birds provide a possibility to study the evolutionary mechanisms behind the highly divergent avian plumage patterns.     

Females discriminate against heterospecific sperm in a natural hybrid zone

When hybridization is maladaptive, species‐specific mate preferences are selectively favored, but low mate availability may constrain species‐assortative pairing. Females paired to heterospecifics may then benefit by copulating with multiple males and subsequently favoring sperm of conspecifics. Whether such mechanisms for biasing paternity toward conspecifics act as important reproductive barriers in socially monogamous vertebrate species remains to be determined. We use a combination of long‐term breeding records from a natural hybrid zone between collared and pied flycatchers (Ficedula albicollis and F. hypoleuca), and an in vitro experiment comparing conspecific and heterospecific sperm performance in female reproductive tract fluid, to evaluate the potential significance of female cryptic choice. We show that the females most at risk of hybridizing (pied flycatchers) frequently copulate with multiple males and are able to inhibit heterospecific sperm performance. The negative effect on heterospecific sperm performance was strongest in pied flycatcher females that were most likely to have been previously exposed to collared flycatcher sperm. We thus demonstrate that a reproductive barrier acts after copulation but before fertilization in a socially monogamous vertebrate. While the evolutionary history of this barrier is unknown, our results imply that there is opportunity for it to be accentuated via a reinforcement‐like process.     

Are incubation costs in female pied flycatchers expressed in humoral immune responsiveness or breeding success?

Although clutch size variation has been a key target for studies of avian life history theory, most empirical work has only focused on the ability of parents to raise their altricial young. In this study, we test the hypothesis that costs incurred during incubation may be an additional factor constraining clutch size in altricial birds. In the pied flycatcher (Ficedula hypoleuca), we manipulated the incubation effort of the female by enlarging and reducing clutch sizes. To manipulate incubation effort only, the original clutch sizes were restored shortly after hatching. We found that fledging success was lower among broods whose clutches were enlarged during incubation. There was, however, no effect of manipulation on female body condition or on their ability to mount a humoral immune response to diphtheria or tetanus toxoid during the incubation or nestling provisioning period. Instead, we found that the original clutch size was related to the immune response so that females with seven eggs had significantly lower primary antibody responses against tetanus compared to those with six eggs. Our results suggest that incubating females are not willing to jeopardise their own condition and immune function, but instead pay the costs of incubating a larger clutch by lower offspring production. The results support the view that costs of producing and incubating eggs may be substantial and hence that these costs are likely to contribute to shaping the optimal clutch size in altricial birds.     

Polygyny and its fitness consequences for primary and secondary female pied flycatchers

In polygynous species with biparental care, the amount of paternal support often varies considerably. In the pied flycatcher (Ficedula hypoleuca), females mated with monogamous males receive more male assistance during the nestling phase than females mated with bigynous males, as the latter have to share their mates with another female. Bigynous males, however, give more support to their primary broods than to their secondary broods. Using a long-term dataset (31 years), the present study revealed that direct reproductive success, i.e. number of fledglings, was lower in females that mated with bigynous males, especially in secondary broods without male assistance, than in females that mated with monogamous males. Secondary broods with male assistance were more affected than primary broods. Female survival was independent of mating status. In primary broods, a delayed compensation for inferior direct reproductive success was found in terms of the number of grandoffspring, a phenomenon that did not occur in secondary broods. Delayed compensation in primary broods refers to indirect effects, i.e. good genes. According to the sexy son hypothesis, genetically superior (i.e. sexy) males may have sons with a higher number of broods belonging to a polygynous breeding status than do sons from broods with a monogamous father. This was indeed the case for sons descending from primary broods, but not for sons descending from secondary broods.