Cost of mobbing call to breeding pied flycatcher, Ficedula hypoleuca

Mobbing signals advertise the location of a stalking predatorto all prey in an area and recruit them into the inspectionaggregation. Such behavior usually causes the predator to moveto another area. However, mobbing calls could be eavesdroppedby other predators. Because the predation cost of mobbing callsis poorly known, we investigated whether the vocalizations ofthe mobbing pied flycatcher, Ficedula hypoleuca, a small holenesting passerine, increase the risk of nest predation. We usedmobbing calls of pied flycatchers to examine if they could lurepredators such as the marten, Martes martes. This predator usuallyhunts by night and may locate its mobbing prey while restingnearby during the day. Within each of 56 experimental plots,from the top of one nest-box we played back mobbing sounds ofpied flycatchers, whereas blank tapes were played from the topof another nest-box. The trials with mobbing calls were carriedout before sunset. We put pieces of recently abandoned nestsof pied flycatchers and a quail, Coturnix coturnix, egg intoeach of the nest-boxes. Nest-boxes with playbacks of mobbingcalls were depredated by martens significantly more than werenest-boxes with blank tapes. The results of the present studyindicate that repeated conspicuous mobbing calls may carry asignificant cost for birds during the breeding season.     

Plumage colour and sexual selection in the pied flycatcher Ficedula hypoleuca

The plumage colour of male pied flycatchers varies on a continuum from brownish and female-like to a conspicuous black-and-white. Males have a conspicuous plumage only during the breeding season, when the mortality rate was low and not correlated with plumage colour. Brownish males breed successfully, and breeding males had no lower annual rate of return than non-breeders. Experiments on male intrusion showed that possession of a cryptic, female-like plumage did not facilitate nest site settlement by such males. Dark males were on average older, arrived earlier, and defended more nestboxes than brown males. However, experiments showed that plumage colour was not a reliable indicator of the outcome of competitive combats between males. These facts argue against several existing hypotheses about variation in male plumage colour. A new explanation is proposed: a bright colour serves to signal presence and thereby reduces territory holding costs. The brownish males arrive only shortly before the females and thus will not benefit as much by being conspicuous as do the black-and-white males that arrive earlier in spring.     

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]     

Nestling testosterone controls begging behaviour in the pied flycatcher, Ficedula hypoleuca

Begging signals and endogenous testosterone (T) levels of young birds have been shown to be positively correlated. If T is causally involved in controlling the level of begging effort, an endocrine control mechanism could explain the evolution of begging as a costly signal reflecting need. We tested experimentally whether elevated circulating T levels enhanced begging behaviour in nestling pied flycatchers, Ficedula hypoleuca. A pilot study confirmed that nestling T levels could be elevated within a natural physiological range using an oral dose of T. After T-dosing, nestling begging behaviour was measured as: i) the duration of begging displays and ii) the maximum height of begging stretches. Our results show that nestling T levels were elevated at 90 min post dosing and that at this time point both measures of begging behaviour were performed more intensely by T-dosed nestlings than controls. Nestling begging displays in response to dosing varied between individuals, which in part was explained either by the date in the breeding season or nestling mass. The results of this study confirm the causal nature of T in controlling nestling begging signals and suggest that it may be part of the mechanism that controls begging behaviour in nestling 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.     

Egg colouration and male parental effort in the pied flycatcher Ficedula hypoleuca

A recent hypothesis posits that the bright colours of many avian eggs may act like signals of female genetic quality or condition to males in species with biparental care, inducing them to work harder for their offspring. We measured the colour of blue eggs of pied flycatchers Ficedula hypoleuca in Central Spain with a spectrophotometer on the day of laying, and also quantified the provisioning effort by males and females during the last days of the nestling period. Both chromaticity coordinates in the CIELAB colour space (blue to yellow, green to red) showed significant associations with male provisioning rates, explaining more than 20% of variation in male parental effort. Male provisioning rates were positively correlated with nestling condition, thereby potentially contributing to female fitness. This evidence is only tentative until experimental confirmation, but suggests that males are affected by the colour of their mates' eggs, a possibility not considered hitherto in the study of sexual selection.     

Pollution related effects on immune function and stress in a free-living population of pied flycatcher Ficedula hypoleuca

We investigated whether exposure to heavy metal pollution affected the immune function of individuals in a free living population of a small insectivorous passerine bird, the pied flycatcher Ficedula hypoleuca . We measured humoral immune responses in two study areas: a polluted area in the vicinity of a copper smelter and a control area far from the smelter. Plasma corticosterone level and blood heterophil/lymphocyte ratio (H/L) were used as more general physiological measures of stress. The immune response of F. hypoleuca was not suppressed by pollution stress. In contrast, we found that F. hypoleuca males showed stronger humoral immune responses to a novel antigen (tetanus toxoid) in the polluted environment than in the unpolluted one. After the immunization of males, numbers of lymphocytes rose significantly more in the polluted area, leading to a smaller H/L ratio than in males from the control area. Females showed no pollution related effects on their immune responses. Corticosterone levels of males and nestlings were not related to pollution levels. Nestlings showed somewhat higher H/L ratios and lower fledging success in the polluted area, both factors indicating increased stress levels in a polluted area. Our results suggest that humoral immune response of male F. hypoleuca may be enhanced under moderate levels of heavy metal pollution. Enhanced immune function may, however, also be costly for birds and the higher humoral immune responses in polluted areas may thus have negative effects on the birds' breeding performance and survival.     

The sexy son hypothesis: data from the pied flycatcher Ficedula hypoleuca

The sexy son hypothesis has been proposed as a possible explanation for polygyny in territorial birds. Females mated with polygynous males are assumed to derive benefits in future generations through their ‘sexy’ sons, and hence they can afford to produce fewer offspring than simultaneously breeding monogamous females, the polygyny threshold thus being reduced. In the pied flycatcher, secondary females are not fully aided by males in feeding the nestlings, and they produce only 65% as many fledglings as do simultaneous monogamous and primary females. We have proposed male deception through polyterritoriality as the explanation for females ending up as secondary females, while some authors have advocated the sexy son hypothesis as an alternative. However, secondary females do not achieve benefits in future generations in this species. Repeatability of male mating status is far too low to grant any significant benefits through grandsons. In fact, offspring hatched in secondary female nests suffer from food shortage and therefore are of poor phenotypic quality with low fledging weight and short tarsus length. Therefore they are likely to enjoy lower reproductive success than offspring born in monogamous nests, as is illustrated by data on the relation between lifetime reproductive success and tarsus length. Altogether the applicability of the sexy son hypothesis is limited since it is based on the unrealistic assumption of relatively high heritability for a character with great influence on male fitness.     

Prehatching maternal investment and offspring immunity in the pied flycatcher (Ficedula hypoleuca)

Maternal investment in offspring immunity via egg quality may be an adaptive evolutionary strategy shaped by natural selection. We investigated how maternal investment in eggs can influence offspring immunity by conducting two experiments. First, we manipulated foraging performance of the mothers before egg laying by attaching a small weight to their back feathers. During the nestling period, we investigated offspring total antibody production at the age of 7 days and after antibody challenge, and conducted a partial cross-fostering design to separate the effects of the experiment and rearing-related variation on offspring immunity. In a separate experiment, partial cross-fostering with antibody challenging without female pied flycatcher manipulation was conducted for another set of nests. Total antibody levels at the age of 7 days were reduced in nestlings of the experimental female pied flycatchers when compared with the set of unmanipulated nests. Maternal investment in the eggs may affect some aspects of offspring immunity during the early nestling period and this investment is costly. However, antibody response to a set of novel antigens (sheep red blood cells) at the end of the nestling period was not affected by the female pied flycatchers treatment. Instead our results suggest that general antibody responsiveness is mainly determined by the rearing environment and total antibody levels before the injection.     

Experimentally reduced male attractiveness increases parental care in the pied flycatcher Ficedula hypoleuca

This study reports effects of experimental manipulations ofreproductive effort and the size of the male's white foreheadpatch (a secondary sexual trait), on provisioning rates, reproductivesuccess, and parental breeding dispersal distance in the piedflycatcher, Ficedula hypoleuca. Parents caring for enlargedbroods resulting from manipulated clutches provisioned nestsat higher rates than parents with reduced broods. Males with a reduced forehead patch fed their nestlings more in relationto males with an unmanipulated forehead patch, and their youngfledging with a longer tarsi. This suggests that males witha reduced attractiveness may perceive their own attractivenessand they devote more time available for parental effort given their poorer prospects in male contest competition and/or femaleattraction for extra-pair copulations. However, their femalesdid not alter their provisioning effort and this runs counterto both the differential allocation and the partner-compensationhypotheses. An artificial decrease in a male secondary sexualtrait led to a wider breeding dispersal distance between successiveyears.     

Seventy new microsatellites for the pied flycatcher, Ficedula hypoleuca and amplification in other passerine birds

The pied flycatcher (Ficedula hypoleuca) is a small migratory passerine bird commonly distributed across Europe which has been the focus of considerable ecological and evolutionary research. Here, we present details of 70 microsatellite markers for the species adding to the six which are currently available. Sixty-six markers were also polymorphic in the closely related collared flycatcher (Ficedula albicollis), while 54 were polymorphic in another related passerine, the bluethroat (Luscinia svecica), and 12 were polymorphic in the more distantly related Siberian jay (Perisoreus infaustus).     

Decline of a montane Mediterranean pied flycatcher Ficedula hypoleuca population in relation to climate

Certain populations of long‐distance migratory birds are suffering declines, which may be attributed to effects of climate change. In this article, we have analysed a long‐term (1991–2015) data set on a pied flycatcher Ficedula hypoleuca population breeding in nest‐boxes in a Mediterranean montane oak forest, exploring the trends in population size due to changes in nestling recruitment, female survival and female immigration. We have related these changes in population parameters to local climate, winter NAO index and to breeding density. During the last 25 yr the population has declined by half, mainly in association with a decrease in nestling mass and structural size which had repercussions on the probability of nestling recruitment to the population. Lower local nestling recruitment in certain years was linked to lower female immigration rate in the same years. On the other hand, the local survival of females remained stable throughout the study period. Laying date and breeding success were negatively affected by local temperatures while breeding, recruitment rate likewise by minimum temperature prior to breeding in April. As minimum April temperatures have increased across the study period, this may have affected recruitment and immigration rates negatively. On the other hand, tarsus length and body mass of nestlings were positively associated with winter NAO index, pointing to more global climatic links. Moreover, there was also a negative temporal trend in body mass of adults, implying increasingly difficult conditions for breeding. Declining recruit production in the study area could be attributed to a mismatch between the timing of arrival and breeding in the population, and the peak of food availability in this area.     

Evidence for the signaling function of egg color in the pied flycatcher Ficedula hypoleuca

A recent hypothesis proposes that the bright colors, especiallyblue and green, of many avian eggs may function as signals offemale or offspring phenotypic quality or condition to malesin species with biparental care, inducing them to allocate moreeffort to their offspring. The pigment determining blue andgreen egg colors is an antioxidant whose availability for eggshellcoloring may be limited. To test the signaling function on aspecies with blue eggs, the pied flycatcher Ficedula hypoleuca,we measured egg color with a spectrophotometer on the day oflaying and obtained two principal components from their reflectancespectra that together explained 99% of variation and representedshell lightness, and hue and saturation, respectively. We alsomeasured female immunocompetence during the nestling periodthrough the response to phytohemagglutinin as a measure of cell-mediatedimmunity and the response to a tetanus vaccination as a measureof humoral immunity. The total amount of immunoglobulins inblood of females and of nestlings before fledging was also estimated.Mean within-clutch egg darkness was positively associated withboth measures of female immunocompetence, while better femalecondition was associated with colors tending away from intermediateand toward short wavelengths. Ageing female laid lighter eggs.The mean within-brood level of nestling IgY was also associatedwith mean within-clutch egg colors tending away from intermediateand toward short wavelengths. Mean egg darkness decreased linearlyduring the laying sequence, suggesting pigment limitation. Maleswere observed frequently visiting nests during the laying period,allowing them to observe eggs before the start of incubation.These results support the signaling hypothesis for explainingbright colors of avian eggs.     

Trade-offs between sexual advertisement and immune function in the pied flycatcher (Ficedula hypoleuca)

Good genes models of sexual selection assume that sexual advertisement is costly and thus the level of advertisement honestly reveals heritable viability. Recently it has been suggested that an important cost of sexual advertisement might be impairment of the functioning of the immune system. In this field experiment we investigated the possible trade-offs between immune function and sexual advertisement by manipulating both mating effort and activity of immune defence in male pied flycatchers. Mating effort was increased in a non-arbitrary manner by removing females from mated males during nest building. Widowed males sustained higher haematocrit levels than control males and showed higher expression of forehead patch height, suggesting that manipulation succeeded in increasing mating effort. Males that were experimentally forced to increase mating effort had reduced humoral immune responsiveness compared with control males. In addition, experimental activation of immune defence by vaccination with novel antigens reduced the expression of male ornament dimensions. To conclude, our results indicate that causality behind the trade-off between immune function and sexual advertisement may work in both directions: sexual activity suppresses immune function but immune challenge also reduces sexual advertisement.     

Nestling testosterone is associated with begging behaviour and fledging success in the pied flycatcher, Ficedula hypoleuca

Animal signals are hypothesized to be costly in order to honestly reflect individual quality. Offspring solicitation signals given by nestling birds are thought to have evolved to advertise either need or individual quality. We tested the potential role of testosterone (T) in controlling the intensity of these signals by measuring begging behaviour as: (i) duration of the begging display and (ii) maximum height of the begging stretch, and by sampling endogenous T levels in nestling blood. We tested nestling pied flycatchers (Ficedula hypoleuca) using well-established experimental paradigm involving transient food deprivation to encourage begging behaviour and then blood-sampled nestlings at the end of these tests for T levels. Our results show that individual nestlings with the most intense begging displays had the highest circulating levels of T immediately after testing. In addition, we found substantial differences between broods in terms of circulating T. Finally, we found evidence that broods with higher levels of T showed increased fledging success, indicating a benefit for increased T production in nestlings. The potential trade-offs involved in T-mediated begging behaviour are discussed.     

Descriptive and experimental evidence for timing-mediated polygyny risk in a pied flycatcher Ficedula hypoleuca population

In polygynous species with biparental care, mates are often acquired in succession. Most research has focussed on the cost of polygyny in secondary females, but primary females may also suffer from reduced paternal care. The likelihood of sharing a male may be higher for early laying females, which could counteract the fitness benefits of breeding early. In this study, we use 12 years of data on pied flycatchers Ficedula hypoleuca, to show that the likelihood of becoming a primary female of a polygynous male declines over the season. Moreover, we provide experimental evidence that early breeding elevates polygyny risk, through an experimental manipulation that introduced early breeding females to a population with later breeding phenology. We found that, independently of breeding date, primary females slightly more often experienced complete brood failures than monogamous females, but did not differ in number of fledged offspring among successful broods or number of locally returning recruits. However, apparent survival in subsequent years was substantially lower in primary females, indicating that they may compensate for reduced male care at the expense of future reproduction. Our study reveals that polygyny risk indeed increases with early breeding and entails a local survival cost for primary females. However, this cost is likely largely outweighed by fitness benefits of early breeding in most years. Hence it is unlikely that the increased polygyny risk of early breeding counteracts the fitness benefits, but it may reduce selection for breeding extremely early.     

Geographical trends in the yolk carotenoid composition of the pied flycatcher (Ficedula hypoleuca)

Carotenoids in the egg yolks of birds are considered to be important antioxidants and immune stimulants during the rapid growth of embryos. Yolk carotenoid composition is strongly affected by the carotenoid composition of the female??s diet at the time of egg formation. Spatial and temporal differences in carotenoid availability may thus be reflected in yolk concentrations. To assess whether yolk carotenoid concentrations or carotenoid profiles show any large-scale geographical trends or differences among habitats, we collected yolk samples from 16 European populations of the pied flycatcher, Ficedula hypoleuca. We found that the concentrations and proportions of lutein and some other xanthophylls in the egg yolks decreased from Central Europe northwards. The most southern population (which is also the one found at the highest altitude) also showed relatively low carotenoid levels. Concentrations of ??-carotene and zeaxanthin did not show any obvious geographical gradients. Egg yolks also contained proportionally more lutein and other xanthophylls in deciduous than in mixed or coniferous habitats. We suggest that latitudinal gradients in lutein and xanthophylls reflect the lower availability of lutein-rich food items in the northern F. hypoleuca populations and in montane southern populations, which start egg-laying earlier relative to tree phenology than the Central European populations. Similarly, among-habitat variation is likely to reflect the better availability of lutein-rich food in deciduous forests. Our study is the first to indicate that the concentration and profile of yolk carotenoids may show large-scale spatial variation among populations in different parts of the species?? geographical range. Further studies are needed to test the fitness effects of this geographical variation.     

Climatic effects on arrival and laying dates in a long-distance migrant, the Collared Flycatcher Ficedula albicollis

Long‐distance migrants may respond to climate change in breeding, wintering or staging area by changing their phenology. The geographical variation in such responses (e.g. coastal vs. continental Europe) and the relative importance of climate at different spatial scales remain unclear. Here we analysed variation in first arrival dates (FADs) and laying dates of the Collared Flycatcher Ficedula albicollis in a central European population, from 1973 to 2002. The North Atlantic Oscillation (NAO) index correlated weakly with local temperature during the laying period. Decreasing spring temperatures until 1980 were associated with a trend towards later laying. The rate of warming (0.2 °C per year) and laying advancement (0.4 days per year) since 1980 are amongst the highest values reported elsewhere. This long‐term trend in laying date was largely explained by the change in climatic factors. The negative effect of local spring temperature on laying was relatively stronger than that of NAO. The number of clutches initiated on a particular day was marginally affected by the temperature 3 days prior to laying and the response of females to daily variation in temperature did not change over years. Correspondence between the average population‐level and the individual‐level responses of laying date to climate variation suggests that the advancement of laying was due to phenotypic plasticity. Despite warmer springs and advanced laying, FADs did not change over years and were not correlated with local spring temperature. Marginal evidence suggests later departure from wintering grounds and faster migration across staging areas in warmer conditions. Advancement of arrival was probably constrained by low local temperatures in early spring just before arrival that have not changed over years. The interval between first arrival and laying has declined since 1980 (0.5 days per year), but the increasing temperature during that period may have kept the food supply approximately unchanged.