Climate change and fitness components of a migratory bird breeding in the Mediterranean region

The increase in spring temperatures in temperate regions over the last two decades has led to an advancing spring phenology, and most resident birds have responded to it by advancing their onset of breeding. The pied flycatcher (Ficedula hypoleuca) is a long‐distance migrant bird with a relatively late onset of breeding with respect to both resident birds and spring phenology in Europe. In the present correlational study, we show that some fitness components of pied flycatchers are suffering from climate change in two of the southernmost European breeding populations. In both montane study areas, temperature during May increased between 1980 and 2000 and an advancement of oak leafing was detected by using the normalized difference vegetation index (NDVI) to assess tree phenology. This might result in an advancement of the peak in availability of caterpillars, the main prey during the nestling stage. Over the past 18 yr, the time of egg laying and clutch size of pied flycatchers were not affected by the increase in spring temperatures in these Mediterranean populations. However, this increase seems to have an adverse effect on the reproductive output of pied flycatchers over the same period. Our data suggest that the mismatch between the timing of peak food supply and nestling demand caused by recent climate change might result in a reduction of parental energy expenditure that is reflected in a reduction of nestling growth and survival of fledged young in our study populations. The data seem to indicate that the breeding season has not shifted and it is the environment that has shifted away from the timing of the pied flycatcher breeding season. Mediterranean pied flycatchers were not able to advance their onset of breeding, probably, because they are constrained by their late arrival date and their restricted high altitude breeding habitat selection near the southern border of their range.     

Effects of latitude on the trade-off between reproduction and moult: a long-term study with pied flycatcher

Long-distance migratory passerine birds are generally time constrained by reproduction and moult, which need to be completed before migration. Breeding and post-nuptial moult may overlap especially under time-constrained conditions (northern latitudes). Here, we analysed the timing of adult moult in relation to latitude, timing of breeding and reproductive effort in pied flycatchers (Ficedula hypoleuca) breeding in four widely separated populations (40-68° N). In males but not females, the proportion of moulting birds while provisioning nestlings increased with increasing latitude. This may suggest that a moult-breeding overlap is a strategy employed by male pied flycatchers to adjust to the short breeding season at northern latitudes. However, the moult-breeding overlap was more pronounced among males in the southernmost study population (Spain). In this population, males may decide not to invest more in reproduction, and start moulting at earlier breeding stage than in northern populations,or, alternatively, birds in the Mediterranean region are time constrained by the hot and dry summer. The trade-off between breeding and post-nuptial moult may be more important in some populations than in others, depending on the latitude of the breeding site. Our results show that a moult-breeding overlap imposes a fitness cost on males in terms of fecundity and breeding success.     

Light‐level geolocators reveal migratory connectivity in European populations of pied flycatchers Ficedula hypoleuca

Understanding what drives or prevents long‐distance migrants to respond to environmental change requires basic knowledge about the wintering and breeding grounds, and the timing of movements between them. Both strong and weak migratory connectivity have been reported for Palearctic passerines wintering in Africa, but this remains unknown for most species. We investigated whether pied flycatchers Ficedula hypoleuca from different breeding populations also differ in wintering locations in west‐Africa. Light‐level geolocator data revealed that flycatchers from different breeding populations travelled to different wintering sites, despite similarity in routes during most of the autumn migration. We found support for strong migratory connectivity showing an unexpected pattern: individuals breeding in Fennoscandia (S‐Finland and S‐Norway) wintered further west compared to individuals breeding at more southern latitudes in the Netherlands and SW‐United Kingdom. The same pattern was found in ring recovery data from sub‐Saharan Africa of individuals with confirmed breeding origin. Furthermore, population‐specific migratory connectivity was associated with geographical variation in breeding and migration phenology: birds from populations which breed and migrate earlier wintered further east than birds from ‘late’ populations. There was no indication that wintering locations were affected by geolocation deployment, as we found high repeatability and consistency in δ¹³C and δ¹⁵N stable isotope ratios of winter grown feathers of individuals with and without a geolocator. We discuss the potential ecological factors causing such an unexpected pattern of migratory connectivity. We hypothesise that population differences in wintering longitudes of pied flycatchers result from geographical variation in breeding phenology and the timing of fuelling for spring migration at the wintering grounds. Future research should aim at describing how temporal dynamics in food availability across the wintering range affects migration, wintering distribution and populations’ capacity to respond to environmental changes.     

The effects of four decades of climate change on the breeding ecology of an avian sentinel species across a 1,500‐km latitudinal gradient are stronger at high latitudes

Global warming affects breeding phenology of birds differentially with latitude, but there is contrasting evidence about how the changing climate influences the breeding of migrating songbirds at their northern breeding range. We investigate the effect of climate warming on breeding time and breeding success of European pied flycatchers Ficedula hypoleuca in Sweden during a period of 36 years using nest reports from bird ringing. To account for the latitudinal variation, we divided Sweden into three latitudinal bands (northern, intermediate, and southern). We applied a sliding window approach to find the most influential period and environment characteristics (temperature, vegetation greenness, and precipitation), using linear mixed models and model averaging. Our results show a long‐term advancement of breeding time related to increasing spring temperature and vegetation greenness during a period before hatching. Northern breeders revealed a larger advancement over the years (8.3 days) compared with southern breeders (3.6 days). We observed a relatively stronger effect of temperature and greenness on breeding time in the north. Furthermore, northern birds showed an increase in breeding success over time, while birds breeding at southern and intermediate latitudes showed reduced breeding success in years with higher prehatching temperatures. Our findings with stronger environment effects on breeding time advancement in the north suggest that pied flycatchers are more responsive to weather cues at higher latitudes. Breeding time adjustment and, potentially, low competition help explain the higher long‐term success observed in the north. Reduced breeding success at more southerly latitudes suggests an inability to match breeding time to very early and warm springs, a fate that with continued climate change could also be expected for pied flycatchers and other long‐distance migrants at their very northern breeding range.     

Linking anti-predator behaviour and habitat quality: group effect in nest defence of a passerine bird

In habitats where the density of breeding individuals is higher, breeding success has been shown to increase with the number of close conspecific and heterospecific neighbours. However, the mechanisms linking habitat quality, group size of prey individuals and offspring defence are poorly known. In this field study, we examined the relationships between habitat quality and parental nest defence behaviour in the pied flycatcher (Ficedula hypoleuca). We found that mobbing is more intense in unmanaged forests where birds breed in more dense and diverse communities than in heavily managed young forests where heterospecific densities are lower. We also found that the mobbing activities of pied flycatchers breeding in unmanaged mature boreal forests attracted more neighbouring prey individuals than in nearby managed forests. This study shows that habitat quality-mediated effects might be responsible for the decreased group size of mobbing birds in managed forests, which may lead to less effective communal defence.     

Climate change, breeding date and nestling diet: how temperature differentially affects seasonal changes in pied flycatcher diet depending on habitat variation

1.?Climate warming has led to shifts in the seasonal timing of species. These shifts can differ across trophic levels, and as a result, predator phenology can get out of synchrony with prey phenology. This can have major consequences for predators such as population declines owing to low reproductive success. However, such trophic interactions are likely to differ between habitats, resulting in differential susceptibility of populations to increases in spring temperatures. A mismatch between breeding phenology and food abundance might be mitigated by dietary changes, but few studies have investigated this phenomenon. Here, we present data on nestling diets of nine different populations of pied flycatchers Ficedula hypoleuca, across their breeding range. This species has been shown to adjust its breeding phenology to local climate change, but sometimes insufficiently relative to the phenology of their presumed major prey: Lepidoptera larvae. In spring, such larvae have a pronounced peak in oak habitats, but to a much lesser extent in coniferous and other deciduous habitats. 2.?We found strong seasonal declines in the proportions of caterpillars in the diet only for oak habitats, and not for the other forest types. The seasonal decline in oak habitats was most strongly observed in warmer years, indicating that potential mismatches were stronger in warmer years. However, in coniferous and other habitats, no such effect of spring temperature was found. 3.?Chicks reached somewhat higher weights in broods provided with higher proportions of caterpillars, supporting the notion that caterpillars are an important food source and that the temporal match with the caterpillar peak may represent an important component of reproductive success. 4.?We suggest that pied flycatchers breeding in oak habitats have greater need to adjust timing of breeding to rising spring temperatures, because of the strong seasonality in their food. Such between-habitat differences can have important consequences for population dynamics and should be taken into account in studies on phenotypic plasticity and adaptation to climate change.     

Translocation as a novel approach to study effects of a new breeding habitat on reproductive output in wild birds

Environmental conditions under which species reproduce have major consequences on breeding success and subsequent fitness. Therefore breeding habitat choice is ultimately important. Studies rarely address the potential fitness pay-offs of alternative natural breeding habitats by experimental translocation. Here we present a new tool to study fitness consequences of free living birds in different habitats. We translocated a migratory passerine, the pied flycatcher (Ficedula hypoleuca), to a novel site, where pairs were subjected to a short stay (2-4 days) in a nest box-equipped aviary before being released. We show that it is technically possible to retain birds in the new area for breeding, allowing the study of reproductive consequences of dispersal under natural conditions. The translocation resulted in an extension of the interval between arrival and egg laying of four days, highlighting the importance of having an adequate control group. Clutch size and nestling parameters did not differ significantly between translocated and unmanipulated females, which suggests that the procedure did not affect birds in their reproductive performance later on. This method could be applied broadly in evolutionary and ecological research, e.g., to study the potential fitness benefits and costs for dispersing to more northern latitudes as a way of adapting to climate change.     

Trade-off between reproduction and moult – a comparison of three Fennoscandian pied flycatcher populations

Organisms that reproduce at high latitudes are assumed to have evolved several adaptations to the short summer. For birds, and especially for long-distance migrants, there is a time constraint because both reproduction and moult must be completed before autumn migration. It has therefore been assumed that birds at northern latitudes must initiate their moult during reproduction more often than birds at low latitudes. To investigate how passerine birds breeding at different latitudes allocate their time between reproduction and moult, we compared timing of these activities during three consecutive breeding seasons in three widely separated populations of the pied flycatcher Ficedula hypoleuca. Our results show that the frequency of individuals with moult-breeding overlap, and moult initiation in relation to breeding stage, varied considerably among populations and years. In all three populations, female moult initiation was restricted to the late nestling period. The males had a more pronounced moult-breeding overlap than the females, but its duration was similar in all three study areas. Thus, there was no evidence for a more pronounced moult-breeding overlap at high compared with low latitudes. These results suggest that pied flycatchers sometimes accept a moult-breeding overlap, but that the time gained by having too extensive an overlap between reproduction and moult does not outweigh the associated costs. Long-distance migrants breeding at northern latitudes apparently experience a trade-off between reproduction and somatic investment during moult. We therefore suggest that a pronounced moult-breeding overlap is not a typical strategy used by long-distance migrants to adjust to the short breeding season at northern latitudes. Received: 7 May 1998 / Accepted: 24 August 1998     

Variation in climate warming along the migration route uncouples arrival and breeding dates

Migratory species are of special concern in the face of global climate change, since they may be affected by changes in the wintering area, along the migration route and at the breeding grounds. Here we show that migration and breeding times of a trans‐Saharan migrant, the pied flycatcher Ficedula hypoleuca, closely follow local temperatures along the migration route and at the breeding grounds. Because of differences in long‐term temperature trends of short within‐spring periods, the migration period and the time interval between migration and breeding dates of this species have extended in SW Finland. Temperatures in northern parts of Central Europe have risen at the time when the first migrants arrive there, facilitating their migration northward. Temperatures later in the spring have not changed, and the last individuals arrive at the same time as before. The timing of breeding has not advanced because temperatures at the breeding site after arrival have not changed. These results show that the pied flycatchers can speed up their migration in response to rising temperatures along the migration route. Our results strongly indicate that the effects of climate change have to be studied at the appropriate time and geographical scales for each species and population concerned.     

Large-scale effect of climate change on breeding parameters of pied flycatchers in Western Europe

Variations in laying date and clutch size of pied flycatchers Ficedula hypoleuca across populations throughout western Europe are examined in relation to climatic fluctuations, measured by the winter North Atlantic Oscillation (NAO) index. Across breeding sites, the winter-NAO index affected laying date such that females lay earlier after warmer and moister winters (positive values of winter NAO-index). Female pied flycatchers breed progressively earlier because presumably the whole breeding season is being shifted, as a direct result of the positive values of winter NAO-index. Moreover, clutch size of pied flycatchers across populations was negatively related to winter NAO-index during the last 50 yr. These analyses controlled for potentially confounding variables such as latitude, longitude, elevation and habitat of each study site. The present study conclude that pied flycatchers across western Europe are breeding earlier and laying smaller clutch sizes and that the most likely cause is a long-term increase in spring temperature. On the other hand, this study shows that climate change may not act uniformly between breeding populations in Western Europe. From those results, this study concludes that northern pied flycatcher populations are more sensitive to climate change than southern populations breeding in montane habitats.     

Positive feedback between ecological and reproductive character displacement in a young avian hybrid zone

Character displacement can reduce costly interspecific interactions between young species. We investigated the mechanisms behind divergence in three key traits-breeding habitat choice, timing of breeding, and plumage coloration-in Ficedula flycatchers. We found that male pied flycatchers became expelled from the preferred deciduous habitat into mixed forest as the superior competitor, collared flycatchers, increased in numbers. The peak in food abundance differs between habitats, and the spatial segregation was paralleled by an increased divergence in timing of breeding between the two species. Male pied flycatchers vary from brown to black with brown coloration being more frequent in sympatry with collared flycatchers, a pattern often proposed to result from selection against hybridization, that is, reinforcement. In contrast to this view, we show that brown male pied flycatchers more often hybridize than black males. Male pied flycatcher plumage coloration influenced the territory obtained in areas of co-occurrence with collared flycatchers, and brown male pied flycatchers experienced higher relative fitness than black males when faced with heterospecific competition. We suggest that allopatric divergence in resource defense ability causes a feedback loop at secondary contact where male pied flycatchers with the most divergent strategy compared to collared flycatchers are favored by selection.     

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.     

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.     

Predation by sparrowhawks Accipiter nisus on male and female pied flycatchers Ficedula hypoleuca in relation to their breeding behaviour and foraging

Bright plumage, song display, and aggressive resource defence in males may cause higher predation on males than on females during the breeding season. However, in birds, higher predation on females is sometimes observed. Parental investment may be high in females (egg-laying, incubation and feeding of offspring), which might lead to a high risk of predation. We studied predation by sparrowhawks Accipiter nisus in relation to behaviour in pied flycatchers Ficedula hypoleuca where breeding males are more conspicuous than females in plumage and behaviour. Male pied flycatchers generally occupied more exposed perches than females. Females were more mobile and foraged more than males, especially prior to and during incubation. During the incubation and nestling stages, when predation on the sexes could be directly compared, sparrowhawks took about the same number of male and female pied flycatchers. During incubation, however, females spent about 77% of the day in the nest and were 4.7 times more vulnerable than males per unit of time available (i.e. outside the nest). A comparison with the chaffinch Fringilla coelebs , where hawks took more females than males, indicates that timing of breeding, foraging behaviour and parental roles of males and females affect predation risk.     

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.     

EVOLUTION OF PLUMAGE COLOR IN MALE PIED FLYCATCHERS (FICEDULA HYPOLEUCA): EVIDENCE FOR FEMALE MIMICRY

We present the first evidence for sexual deception by female mimicry in birds. Using live, caged birds we show that territorial male pied flycatchers behave aggressively toward bright-colored males but display sexually toward female-like male intruders. We also show that the males that are fooled are those that lack recent sexual experience. All male pied flycatchers are dull-colored in winter. It is possible that young males are more constrained during the spring molt than older males since the former are more dull-colored in spring. According to the molt-constraints hypothesis a subadult plumage would be maladaptive in the breeding season. Analysis of male settling pattern at breeding sites in spring suggests that brownish males are allowed to settle closer to already-established males than dark-colored males. This result suggests an adaptive value of having a subadult plumage color, in particular for young males arriving late from spring migration. However, we also show that mimicry incurs a cost, that of increased aggression from females, which may explain why female-like males have reduced mating success.     

Variation in the hematocrit of a passerine bird across life stages is mainly of environmental origin

The heritability of the hematocrit in adult, breeding pied flycatchers Ficedula hypoleuca is examined in a southern European population across seven years to see the consistency, or lack thereof, of patterns found with the trait at fledgling age where no significant heritability could be detected. While the across-years repeatability of the trait in adult, breeding birds was low but significant, heritabilities based on adult parent-adult offspring regressions controlling for assortative mating and full-sibling comparisons did not differ significantly from zero. Neither were heritability estimates affected by selection on fledgling hematocrit, as it was unrelated to local recruitment. There was no relationship between fledgling and adult hematocrit, suggesting that both behave as phenotypically plastic, different traits. This is the first study testing for the heritability of a physiological trait in birds with data from adult, free-ranging individuals.     

Variation of lymphoid activity in the spleen of a migratory bird,the pied flycatcher (Ficedula hypoleuca; Aves,passeriformes)

The size and microscopic structure of the spleen of the migratory pied flycatcher (Ficedula hypoleuca) show marked changes during the reproductive cycle. Upon the spring return to their northern breeding sites, the birds have a small spleen with little lymphoid activity and a poorly developed red pulp. During the breeding period the volume of red and white pulp increases, the number and distinctness of lymphoid follicles (germinal centres) in the white pulp increase, and groups of cells with intensely basophilic cytoplasm, probably B cells (plasma cells), appear. The findings suggest that the immune system of the adult pied flycatcher is activated during periods when it is bound to the nest. Young flycatchers beginning their autumn migration also show a marked increase of lymphoid activity in the spleen.     

Natal dispersal based on past and present environmental phenology in the pied flycatcher (Ficedula hypoleuca)

Natal dispersal allows individuals to reach suitable breeding sites. The effect of present plant phenology as a cue for dispersal into areas with favourable stages of development has been well established across avian and mammalian taxa. However, the effect of past experience is less understood. We studied the effect of past and present phenology of the environment on the direction and distance of natal dispersal in a passerine bird, the pied flycatcher (Ficedula hypoleuca). We monitored spring settlement of local recruits in six nest box plots along a 10-km stretch of a south-north gradient of plant and caterpillar food development. We found that males used both past experience of caterpillar phenology from early life and actual plant phenology during the recruitment season as independent cues for breeding settlement. Males that had experienced a mismatch with the caterpillar food peak as a nestling, and/or those that arrived late in the spring in the recruitment year, moved north of their natal site, whereas males that had experienced a better match with the caterpillars as a nestling, and/or those that migrated earlier in the spring, settled at a similar site or more to the south. In females, no such effects were found, suggesting that the usage of phenological cues is sex specific. In summary, tracking environmental phenology by natal dispersal may represent an effective mechanism for settling in new favourable areas, and may thus potentially cause rapid change of a species’ geographical breeding range in response to climate change.     

Ectoparasites,nest site choice and breeding success in the pied flycatcher

It has recently been suggested that nest box studies might bias the measurement of behavioural and life-history traits, because the removal of old nests may reduce the load of ectoparasites. This experimental artefact may have notable effects on nest site choice and breeding success in cavity-breeding birds. We tested (i) if pied flycatchers Ficedula hypoleuca prefer clean nest boxes and (ii) if old nest material affects the number of parasites and the breeding success of pied flycatchers. In the first experiment we offered birds one cleaned nest box and one nest box with old nest material from the previous year. The two nest boxes were placed in very similar sites near each other. In this experiment all pied flycatchers clearly preferred dirty nest boxes. In the second part of the study we distributed clean nest boxes and dirty ones on the same study area. After breeding was over we counted the number of fleas Ceratophyllus gallinae in the nest material. This flea species was the most abundant and probably the most hazardous parasite in the nests. Surprisingly, we found that there were significantly more fleas in the nest boxes with nests of the current year only than in the boxes with nests of both current and previous year. This might explain the preference for the dirty boxes. However, our results do not indicate that the number of fleas affects breeding success in the pied flycatcher.