Migratory Pied Flycatcher Research Articles

Temperature synchronizes temporal variation in laying dates across European hole-nesting passerines.

Identifying the environmental drivers of variation in fitness-related traits is a central objective in ecology and evolutionary biology. Temporal fluctuations of these environmental drivers are often synchronized at large spatial scales. Yet, whether synchronous environmental conditions can generate spatial synchrony in fitness-related trait values (i.e., correlated temporal trait fluctuations across populations) is poorly understood. Using data from long-term monitored populations of blue tits (Cyanistes caeruleus, n = 31), great tits (Parus major, n = 35), and pied flycatchers (Ficedula hypoleuca, n = 20) across Europe, we assessed the influence of two local climatic variables (mean temperature and mean precipitation in February-May) on spatial synchrony in three fitness-related traits: laying date, clutch size, and fledgling number. We found a high degree of spatial synchrony in laying date but a lower degree in clutch size and fledgling number for each species. Temperature strongly influenced spatial synchrony in laying date for resident blue tits and great tits but not for migratory pied flycatchers. This is a relevant finding in the context of environmental impacts on populations because spatial synchrony in fitness-related trait values among populations may influence fluctuations in vital rates or population abundances. If environmentally induced spatial synchrony in fitness-related traits increases the spatial synchrony in vital rates or population abundances, this will ultimately increase the risk of extinction for populations and species. Assessing how environmental conditions influence spatiotemporal variation in trait values improves our mechanistic understanding of environmental impacts on populations.

Spatial consistency in drivers of population dynamics of a declining migratory bird.

Many migratory species are in decline across their geographical ranges. Single-population studies can provide important insights into drivers at a local scale, but effective conservation requires multi-population perspectives. This is challenging because relevant data are often hard to consolidate, and state-of-the-art analytical tools are typically tailored to specific datasets. We capitalized on a recent data harmonization initiative (SPI-Birds) and linked it to a generalized modelling framework to identify the demographic and environmental drivers of large-scale population decline in migratory pied flycatchers (Ficedula hypoleuca) breeding across Britain. We implemented a generalized integrated population model (IPM) to estimate age-specific vital rates, including their dependency on environmental conditions, and total and breeding population size of pied flycatchers using long-term (34-64 years) monitoring data from seven locations representative of the British breeding range. We then quantified the relative contributions of different vital rates and population structure to changes in short- and long-term population growth rate using transient life table response experiments (LTREs). Substantial covariation in population sizes across breeding locations suggested that change was the result of large-scale drivers. This was supported by LTRE analyses, which attributed past changes in short-term population growth rates and long-term population trends primarily to variation in annual survival and dispersal dynamics, which largely act during migration and/or nonbreeding season. Contributions of variation in local reproductive parameters were small in comparison, despite sensitivity to local temperature and rainfall within the breeding period. We show that both short- and long-term population changes of British breeding pied flycatchers are likely linked to factors acting during migration and in nonbreeding areas, where future research should be prioritized. We illustrate the potential of multi-population analyses for informing management at (inter)national scales and highlight the importance of data standardization, generalized and accessible analytical tools, and reproducible workflows to achieve them.

Territory‐level temperature influences breeding phenology and reproductive output in three forest passerine birds

Temperature plays an important role in determining the breeding phenology of birds in temperate climates, with higher spring temperatures associated with earlier breeding. However, the effect of localised territory‐scale temperature variations is poorly understood, with relationships between temperature and breeding phenology mostly studied using coarse‐grained climatic indices. Here, we interpolate spring temperatures recorded at 150‐m2 grid intersections encompassing 417 ha of forest to examine the influence of territory‐scale temperature, and its interaction with mean annual temperature, on territory selection, breeding phenology, clutch size and fledging success for three co‐occurring single‐brooded passerine birds using data from 672 nests over four years. All species exhibited significant trends in reproductive traits associated with territory‐scale temperature. Pied flycatchers Ficedula hypoleuca settled in cooler territories first, where they raised more fledglings. Blue tits Cyanistes caeruleus laid larger clutches in warmer territories in warm years and always laid earlier at warmer territories irrespective of annual temperature variation. Contrastingly, pied flycatcher and wood warbler Phylloscopus sibilatrix breeding phenology was earlier at warmer territories in cool years and cooler territories in warm years, with wood warbler clutch size responding similarly to this interaction. Greater previous breeding experience and higher rates of historical territory occupancy (territory quality) also predicted earlier breeding phenology and higher fledging success for pied flycatchers. We suggest that the migratory pied flycatcher and wood warbler are best synchronised with their prey availability in cooler years at a local population level. However resident blue tits match local phenology across all years, which is potentially advantageous under warmer predicted climate change scenarios. We conclude that temperature at the territory scale can be an important driver of settlement and breeding phenology and influence reproductive traits.

Evolutionary Response to Climate Change in Migratory Pied Flycatchers.

Climate change is rapidly advancing spring phenology [1-3] but at different rates in different species [1, 4]. Whether these advances are solely driven by phenotypic plasticity [2, 5] or also involve evolution is hotly debated (e.g., [5-7]). In some species, including avian long-distance migrants, plastic responses to early springs may be constrained by inherited circannual timing programs [8, 9], making evolutionary adjustment theonly viable mechanism for keeping pace withshifting phenology [5, 10]. This constraint may becontributing to population declines in migratory species [5, 10-12]. To test whether a migrant's timing program has evolved [10, 12], wereplicated an experimental study of the annual cycle of long-distance migratory pied flycatchers (Ficedula hypoleuca) after 21 years of warming. Flycatchers are a model for studying constrained ecological responses to climate change [6, 10, 12, 13]. We show that the phase of the flycatcher circannual clock controlling spring moult, migration, and reproductive timing advanced by 9days. A nearby wild population mirrored these changes, concurrently advancing egg-laying by 11days. Furthermore, the time window during which wild flycatcher reproductive timing was most sensitive to ambient temperature advanced by 0.8days year-1. These results support a role of phenotypic evolution [14] in changing spring phenology [15, 16]. We suggest that the timing programs oflong-distance migratory birds may have greater adaptive potential than previously thought, leaving some scope for evolutionary rescue in a changing climate.

Climate Change May Affect Fatal Competition between Two Bird Species

Climate warming has altered phenologies of many taxa [1, 2], but the extent differs vastly between [3,4] and within trophic levels [5-7]. Differential adjustment to climate warming within trophic levels may affect coexistence of competing species, because relative phenologies alter facilitative and competitive outcomes [8, 9], but evidence for this is scant [10, 11]. Here, we report on two mechanisms through which climate change may affect fatal interactions between two sympatric passerines, the resident great tit Parus major and the migratory pied flycatcher Ficedula hypoleuca, competing for nest sites. Spring temperature more strongly affected breeding phenology of tits than flycatchers, and tits killed more flycatchers when flycatcher arrival coincided with peak laying in the tits. Ongoing climate change may diminish this fatal competition if great tit and flycatcher phenologies diverge. However, great tit density increased after warm winters, and flycatcher mortality was elevated when tit densities were higher. Consequently, flycatcher males in synchronous and high-tit-density years suffered mortality by great tits of up to 8.9%. Interestingly, we found no population consequences of fatal competition, suggesting that mortality predominantly happened among surplus males. Indeed, late-arriving males are less likely to find a partner [12], and here we show that such late arrivers are more likely to die from competition with great tits. We conclude that our breeding population is buffered against detrimental effects of competition. Nevertheless, we expect that if buffers are diminished, population consequences of interspecific competition may become apparent, especially after warm winters that are benign to resident species. VIDEO ABSTRACT.

Nosy neighbours: large broods attract more visitors. A field experiment in the pied flycatcher, Ficedula hypoleuca.

Life is uncertain. To reduce uncertainty and make adaptive decisions, individuals need to collect information. Individuals often visit the breeding sites of their conspecifics (i.e., "prospect"), likely to assess conspecifics' reproductive success and to use such information to identify high-quality spots for future breeding. We investigated whether visitation rate by prospectors and success of visited sites are causally linked. We manipulated the reproductive success (enlarged, reduced, and control broods) in a nest-box population of migratory pied flycatchers, Ficedula hypoleuca, in Finland. We measured the visitation rates of prospectors at 87 nest-boxes continuously from manipulation (day 3 after hatching) to fledging. 302 adult pied flycatchers prospected 9194 times on these manipulated nests (at least 78% of detected prospectors were successful breeders). While the number of visitors and visits was not influenced by the relative change in brood size we induced, the resulting absolute brood size predicted the prospecting behaviour: the larger the brood size after manipulation, the more visitors and visits a nest had. The parental provisioning rate at a nest and brood size pre-manipulation did not predict the number of visitors or visits post-manipulation. More visitors, however, inspected early than late nests and broods in good condition. Our study suggests that individuals collect social information when visiting conspecific nests during breeding and provides evidence that large broods attract more visitors than small broods. We discuss the results in light of individual decision-making by animals in their natural environments.

Competitor phenology as a social cue in breeding site selection.

Predicting habitat quality is a major challenge for animals selecting a breeding patch, because it affects reproductive success. Breeding site selection may be based on previous experience, or on social information from the density and success of competitors with an earlier phenology. Variation in animal breeding phenology is often correlated with variation in habitat quality. Generally, animals breed earlier in high-quality habitats that allow them to reach a nutritional threshold required for breeding earlier or avoid nest predation. In addition, habitat quality may affect phenological overlap between species and thereby interspecific competition. Therefore, we hypothesized that competitor breeding phenology can be used as social cue by settling migrants to locate high-quality breeding sites. To test this hypothesis, we experimentally advanced and delayed hatching phenology of two resident tit species on the level of study plots and studied male and female settlement patterns of migratory pied flycatchers Ficedula hypoleuca. The manipulations were assigned at random in two consecutive years, and treatments were swapped between years in sites that were used in both years. In both years, males settled in equal numbers across treatments, but later arriving females avoided pairing with males in delayed phenology plots. Moreover, male pairing probability declined strongly with arrival date on the breeding grounds. Our results demonstrate that competitor phenology may be used to assess habitat quality by settling migrants, but we cannot pinpoint the exact mechanism (e.g. resource quality, predation pressure or competition) that has given rise to this pattern. In addition, we show that opposing selection pressures for arrival timing may give rise to different social information availabilities between sexes. We discuss our findings in the context of climate warming, social information use and the evolution of protandry in migratory animals.

Carry-over effects of conditions at the wintering grounds on breeding plumage signals in a migratory bird: roles of phenotypic plasticity and selection.

To understand the consequences of ever-changing environment on the dynamics of phenotypic traits, distinguishing between selection processes and individual plasticity is crucial. We examined individual consistency/plasticity in several male secondary sexual traits expressed during the breeding season (white wing and forehead patch size, UV reflectance of white wing patch and dorsal melanin coloration) in a migratory pied flycatcher (Ficedula hypoleuca) population over an 11-year period. Furthermore, we studied carry-over effects of three environmental variables (NAO, a climatic index; NDVI, a vegetation index; and rainfall) at the wintering grounds (during prebreeding moult) on the expression of these breeding plumage traits of pied flycatcher males at individual and population levels. Whereas NAO correlates negatively with moisture in West Africa, NDVI correlates positively with primary production. Forehead patch size and melanin coloration were highly consistent within individuals among years, whereas the consistency of the other two traits was moderate. Wing patch size decreased with higher NAO and increased with higher rainfall and NDVI at the individual level. Interestingly, small-patched males suffered lower survival during high NAO winters than large-patched males, and vice versa during low NAO winters. These counteracting processes meant that the individual-level change was masked at the population level where no relationship was found. Our results provide a good example of how variation in the phenotypic composition of a natural population can be a result of both environment-dependent individual plasticity and short-term microevolution. Moreover, when plasticity and viability selection operate simultaneously, their impacts on population composition may not be evident.

Do Pied Flycatchers Use Personal or Social Information for Replacement Clutch Decisions? A Field Experiment

Life is a continuous stream of decisions: organisms are repeatedly confronted with multiple options from which to choose. To make the best decisions and maximise their fitness, individuals need to collect information: from direct interactions with the environment (personal information) or from observing other individuals interacting with the environment (social information). Yet, very little is known about the details of decision‐making by animals in their natural environments, including the sources of information they use in the process. We set out to determine the relative importance of social and personal information in breeding habitat decisions in the migratory pied flycatcher, Ficedula hypoleuca. In a field experiment in Finland, we manipulated flycatcher breeding success and then allowed individuals to choose among breeding sites labelled with artificial cues (arbitrary symbols) associated with their own (manipulated) and neighbour's reproductive success, respectively, for laying a replacement clutch. Birds did not appear to distinguish among the symbols representing their own, their neighbour's or a neutral symbol, indicating that they did not use either information source when deciding about a replacement clutch. Also, the choice did not influence subsequent investment into breeding (clutch size). This may suggest that pied flycatchers utilise other cues (e.g. breeding success or predation risk on larger scales) when having to make a decision about replacement clutches. We discuss our results in light of constraints imposed by a short breeding season of migratory birds.

Effects of Habitat on Breeding Success in a Declining Migrant Songbird: the Case of Pied FlycatcherFicedula hypoleuca

Habitat is a key determinant of breeding success in hole-nesting birds. Identifying the factors that influence breeding success is important in understanding nest-site selection behaviour and devising appropriate conservation strategies. This is especially true for declining species like the migratory Pied Flycatcher Ficedula hypoleuca. Here, I analyse the effect of 24 habitat variables on clutch size, hatching success and fledging success for 137 Pied Flycatcher nests in Gloucestershire, UK, using volunteer-collected data from a 5-year period. More successful nests tended to be located in areas with a lower density of mature trees but abundant saplings. Tree and sapling species richness was also important. Success was positively related to abundance of Oak Quercus robur and Silver Birch Betula pendula and negatively related to Beech Fagus sylvatica, Sycamore Acer pseudoplatanus and Bracken Pteridium aquilinum. Success was lower in boxes facing south-southwest and higher in boxes located on sorter trees. Despite Pied Flycatchers often being regarded as birds of grazed (open) woodland, success was not related directly to grazing. Close proximity to footpaths was associated with significantly lower clutch size, numbers of young to fledge, and percentage success, while close proximity to water was associated with increased success at all stages of breeding. This is a single-site study and the generality of these findings at other sites cannot be assumed without empirical testing. However, the results provide useful additional insight into success-habitat interactions in this species that, to some extent, challenge the general view of Pied Flycatchers, in the UK at least, as grazed woodland specialists.

Long‐distance dispersal in migratory pied flycatchers Ficedula hypoleuca is relatively common between the UK and the Netherlands

Long‐distance dispersal can potentially have important consequences for evolutionary change, but is difficult to quantify. We present quantitative estimates of natal dispersal between the UK and the Netherlands in a long‐distance migratory bird, the pied flycatcher. Due to over 90 000 individual ringed adults caught and 730 000 ringed nestlings we are able to estimate that dispersal of young born in the UK to breeding in the Netherlands occurs on average 43 times yr−1, and probably even more recently. We estimated that between 2000 and 2009 about 0.70% of the Dutch adult population could be immigrants from the UK. No cases of dispersal from the Netherlands to the UK were observed. Dispersing individuals bring new genes to the Netherlands, as males in the UK have a darker plumage than Dutch males. We found a good qualitative match between the proportion of dark males breeding in two Dutch populations and the estimated immigration rate from the UK. This and potentially other genetic differences may allow for new evolutionary directions if these genes are beneficial in the new population. The causes of dispersal are unknown, but it is striking that especially birds from the northern range limit dispersed.

Learning what (not) to do: testing rejection and copying of simulated heterospecific behavioural traits

Animals can copy behaviour of heterospecifics (interspecific social learning), but it is not known whether social-learning strategies postulated for conspecific contexts, such as selectively copying individuals (or behaviours) that are more successful or common than the observer, apply here. A recent study found evidence for biased interspecific acquisition of nest site feature preference depending on observed fitness of the demonstrator (clutch size). We experimentally tested whether migratory pied flycatcher, Ficedula hypoleuca, females, given a choice between two novel alternative behavioural traits of nest site feature choice, copy or reject the experimentally induced choice exhibited by simulated resident tit (Parus spp.) nests, when those nests portray a high or low fitness correlate (clutch size). Flycatchers were more likely to choose the opposite trait when the exhibited choice was associated with low simulated tit clutch size, demonstrating active rejection. Flycatchers had a strong overall preference to take over the tit nest site. We conclude that animals in the wild can respond to observable heterospecific fitness correlates when making decisions. Our experiment confirmed the existence of a strategy to reject behaviours exhibited by poorly performing individuals, complementing the already proposed social-learning strategies. By affecting the niche overlap of co-occurring species utilizing similar resources, interspecific social learning may affect species interactions and community structure.

Territory Choice of Pied Flycatchers is Not Based on Induced Cues of Herbivore Damaged Trees~!2010-04-09~!2010-06-01~!2010-07-20~!

Passerine birds use a variety of indirect cues to make territory location decisions. These birds can also distinguish herbivore-damaged plants from undamaged ones during foraging, even when they cannot see the herbivorous larvae or damaged leaves. To test the possibility that also the territory choice of passerines is affected by herbivore- induced plant cues, we established territories with and without indirect cues of herbivore presence for migratory pied flycatchers (Ficedula hypoleuca) at the time of their arrival. Half of the territories had folivorous moth larvae hidden inside mesh bags to defoliate small trees (Betula spp.) and half had only empty mesh bags on trees. Hidden herbivory on the trees did not affect the mean date of territory choice by either male or female birds. Nonetheless, there was a trend that females, but not males, chose the territories in the same order in two consecutive years. Thus, it seems that pied flycatchers do not use indirect cues of larval presence as a basis for their choice of territory, but possibly some more general environmental cues.

Evidence for differential maternal allocation to eggs in relation to manipulated male attractiveness in the pied flycatcher (Ficedula hypoleuca)

We present evidence of differential maternal allocation to eggs in response to manipulated male attractiveness in the migratory pied flycatcher (Ficedula hypoleuca). We manipulated the size of a male secondary sexual trait, the white forehead patch, right after male arrival to the breeding area and before female arrival. Patch size was (1) enlarged to the maximum observed in the population, (2) reduced by 40% or (3) kept constant by painting with indelible felt markers over the natural feather patch. Male behaviour was affected by the experimental manipulation, as individuals with enlarged patches performed more approaches to the nestbox in response to song playback during the territory occupation and nest-site presentation phases. Females paired with males with reduced forehead patches laid significantly smaller eggs than those paired with males in the control and enlarged-patch treatments. Laying date and clutch size did not differ among the experimental groups. We discuss that manipulations of ornaments designed to study differential allocation at laying should reduce as well as enlarge their expression.

Climate change and population declines in a long-distance migratory bird

Phenological responses to climate change differ across trophic levels, which may lead to birds failing to breed at the time of maximal food abundance. Here we investigate the population consequences of such mistiming in the migratory pied flycatcher, Ficedula hypoleuca. In a comparison of nine Dutch populations, we find that populations have declined by about 90% over the past two decades in areas where the food for provisioning nestlings peaks early in the season and the birds are currently mistimed. In areas with a late food peak, early-breeding birds still breed at the right time, and there is, at most, a weak population decline. If food phenology advances further, we also predict population declines in areas with a late food peak, as in these areas adjustment to an advanced food peak is insufficient. Mistiming as a result of climate change is probably a widespread phenomenon, and here we provide evidence that it can lead to population declines.

The effect of climate change on the correlation between avian life‐history traits

AbstractThe ultimate reason why birds should advance their phenology in response to climate change is to match the shifting phenology of underlying levels of the food chain. In a seasonal environment, the timing of food abundance is one of the crucial factors to which birds should adapt their timing of reproduction. They can do this by shifting egg‐laying date (LD), and also by changing other life‐history characters that affect the period between laying of the eggs and hatching of the chicks. In a long‐term study of the migratory Pied Flycatcher, we show that the peak of abundance of nestling food (caterpillars) has advanced during the last two decades, and that the birds advanced their LD. LD strongly correlates with the timing of the caterpillar peak, but in years with an early food peak the birds laid their eggs late relative to this food peak. In such years, the birds advance their hatching date by incubating earlier in the clutch and reducing the interval between laying the last egg to hatching of the first egg, thereby partly compensating for their relative late LD. Paradoxically, they also laid larger clutches in the years with an early food peak, and thereby took more time to lay (i.e. one egg per day). Clutch size therefore declined more strongly with LD in years with an early food peak. This stronger response is adaptive because the fitness of an egg declined more strongly with date in early than in late years. Clearly, avian life‐history traits are correlated and Pied Flycatchers apparently optimize over the whole complex of the traits including LD, clutch size and the onset of incubation. Climate change will lead to changing selection pressures on this complex of traits and presumably the way they are correlated.

Climatic effects on timing of spring migration and breeding in a long‐distance migrant, the pied flycatcher Ficedula hypoleuca

Climate change has advanced the breeding dates of many bird species, but for few species we know whether this advancement is sufficient to track the advancement of the underlying levels of the food chain. For the long‐distance migratory pied flycatcher Ficedula hypoleuca the advancement in breeding time has been insufficient to maintain the synchrony with their main food sources. The timing of arrival in the breeding areas from their African wintering grounds is likely to constrain the advancement of breeding date. We hypothesise that this is because in Africa they cannot predict the advancement of spring in their breeding habitat. However, long‐distance migrants may advance their arrival time by migrating faster when circumstances en route are favourable. In this study we show that both arrival and breeding date depend on temperatures at their main North African staging grounds, as well as on temperature at the breeding grounds. Male arrival and average laying date were not correlated, but the positive effect of temperature in North Africa on breeding dates suggests that breeding date is indeed constrained by arrival of females. Long‐distance migrants thus are able to adjust arrival and hence breeding by faster spring migration, but the degree of adjustment is probably limited as timing schedules in spring are tight. Furthermore, as climate change is affecting temperatures differently along the migratory flyway and the breeding areas, it is unlikely that arrival dates are advanced at the same rate as the timing of breeding should advance, given the advancement of the underlying levels of the food chain.

Adjustment to climate change is constrained by arrival date in a long-distance migrant bird.

Spring temperatures in temperate regions have increased over the past 20 years, and many organisms have responded to this increase by advancing the date of their growth and reproduction. Here we show that adaptation to climate change in a long-distance migrant is constrained by the timing of its migratory journey. For long-distance migrants climate change may advance the phenology of their breeding areas, but the timing of some species' spring migration relies on endogenous rhythms that are not affected by climate change. Thus, the spring migration of these species will not advance even though they need to arrive earlier on their breeding grounds to breed at the appropriate time. We show that the migratory pied flycatcher Ficedula hypoleuca has advanced its laying date over the past 20 years. This temporal shift has been insufficient, however, as indicated by increased selection for earlier breeding over the same period. The shift is hampered by its spring arrival date, which has not advanced. Some of the numerous long-distance migrants will suffer from climate change, because either their migration strategy is unaffected by climate change, or the climate in breeding and wintering areas are changing at different speeds, preventing adequate adaptation.

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.

Night sky orientation of migratory pied flycatchers raised in different magnetic fields

To test whether the initial night sky orientation response of migratory pied flycatchers (Ficedula hypoleuca) is calibrated from the ambient magnetic field experienced by birds during their first summer, three groups of pied flycatchers were hand-reared and then held under different magnetic field conditions during the course of the summer. All groups were held outdoors and given full exposure to the day and night sky. One group was exposed to the local earth's magnetic field. A second group was exposed to a magnetic field of local earth strength, local earth inclination shifted 105° counter-clockwise relative to the local earth's field. The last group was exposed to a vertical, and thus nondirectional magnetic field.