Marko Mägi

Geographic patterns of genetic differentiation and plumage colour variation are different in the pied flycatcher (Ficedula hypoleuca)

The pied flycatcher is one of the most phenotypically variable bird species in Europe. The geographic variation in phenotypes has often been attributed to spatial variation in selection regimes that is associated with the presence or absence of the congeneric collared flycatcher. Spatial variation in phenotypes could however also be generated by spatially restricted gene flow and genetic drift. We examined the genetic population structure of pied flycatchers across the breeding range and applied the phenotypic QST (PST)–FST approach to detect indirect signals of divergent selection on dorsal plumage colouration in pied flycatcher males. Allelic frequencies at neutral markers were found to significantly differ among populations breeding in central and southern Europe whereas northerly breeding pied flycatchers were found to be one apparently panmictic group of individuals. Pairwise differences between phenotypic (PST) and neutral genetic distances (FST) were positively correlated after removing the most differentiated Spanish and Swiss populations from the analysis, suggesting that genetic drift may have contributed to the observed phenotypic differentiation in some parts of the pied flycatcher breeding range. Differentiation in dorsal plumage colouration however greatly exceeded that observed at neutral genetic markers, which indicates that the observed pattern of phenotypic differentiation is unlikely to be solely maintained by restricted gene flow and genetic drift.

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.

Low Reproductive Success of Great Tits in the Preferred Habitat: A Role of Food Availability

Abstract: Habitat-related variation has been revealed in the seasonal reproductive patterns of great tits inhabiting mosaics of deciduous woodland fragments and managed coniferous forests. The number and quality of offspring tend to be higher in the non-preferred coniferous habitat compared with the preferred deciduous habitat. We explored whether these patterns can be explained by variation in food abundance and/or parental provisioning ability. Frass fall seemed not to be a reliable measure of the seasonal dynamics of nestling feeding conditions, although it is widely used for this purpose. No habitat-related differences were found in the tendency of parents to increase provisioning frequency in response to increased hunger levels of nestlings, suggesting that provisioning frequency as such is not a limiting factor for nestling growth. Higher feeding rates in deciduous habitat were associated with lower proportions of high-quality food items among prey delivered to offspring. These findings confirm that relatively high nestling feeding rates in birds may reflect the low quality of available food rather than the quality of parental care or an abundance of food in the environment. The results also indicate that deciduous forest habitat, though preferred by tits, may sometimes provide poorer brood-rearing conditions than the non-preferred, coniferous habitat. We suggest that the great tits preference for deciduous habitat, which presumably evolved in more southern regions, may be maladaptive in northern regions where deciduous woods are mainly young, secondary stands of alder and birch. Nomenclature: Tutin et al., 1993; Dickinson, 2003.

Seasonal mortality trends in tree-feeding insects: a field experiment

Abstract 1. The majority of general life‐history models treat the environment as being invariable through time, even though temporal variation in selective agents could dramatically change the outcomes, e.g. in terms of optimal size and time at maturity. For herbivorous insects, seasonal differences in food quality are reasonably well described, but seasonal dynamics of top‐down selective forces are poorly documented.

Long-term consequences of early ontogeny in free-living Great Tits Parus major

Environmental factors during early development may have profound effects on subsequent life-history traits in many bird species. In wild birds, sex-specific effects of early ontogeny on natal dispersal and future reproduction are not well understood. The objective of this work was to determine whether hatching date and pre-fledging mass and condition of free-living Great Tits Parus major have any subsequent effect on individuals’ natal dispersal and reproductive performance at first breeding. Both males and females dispersed longer distances in coniferous than in deciduous forests, while dispersal was condition-dependent only in males (heavier as nestlings dispersed farther). In females, mass and condition at pre-fledging stage correlated significantly with clutch size, but not with subsequent reproductive performance as measured by fledging success or offspring quality. In contrast, heavier males as nestlings had higher future fledging success and heavier offspring in their broods compared with those in worse condition as nestlings. The hatching date of female as well as male parents was the only parental parameter related to the number of eggs hatched at first breeding. These results indicate that pre-fledging mass and condition predict subsequent fitness components in this bird species. We suggest that sex-specific relationships between a disperser’s condition and its selectivity with respect to breeding habitat and subsequent performance need to be considered in future models of life-history evolution.

Calcium availability affects bone growth in nestlings of free‐living great tits (Parus major), as detected by plasma alkaline phosphatase

Recent studies have revealed that calcium limitation of avian reproduction may be a widespread phenomenon, affecting both egg properties and chick development. The effect of calcium shortage on the final body size of fledglings is usually rather weak, possibly owing to compensatory growth. Achieving full skeletal size is not, however, a reliable indication of complete ossification and it is possible that chicks with similar tarsus lengths are in different stages of skeletal development. We hypothesized that measuring plasma activity of the bone alkaline phosphatase (ALP), a highly specific marker for bone calcification, may reveal subtle developmental differences in full-grown fledglings, having experienced different levels of calcium availability during growth. In two seasons, a number of pairs of great tit Parus major were provided with calcium-rich material during the nestling period, while others were not supplemented (controls). While no significant differences in size of fledglings were detected between groups, bone-ALP activity at the pre-fledging stage was lower in the calcium-provided nestlings than in the control nestlings. This may indicate that supplemented chicks had completed the rapid phase of bone formation, but this process was delayed in controls. Measuring ALP as a marker of skeletal development expands our knowledge of how delayed skeletal development of chicks can result in protraction of the nestling period, thereby reducing the breeding success of adult birds.

Habitat differences in allocation of eggs between successive breeding attempts in great tits (Parus major)

Abstract: The effect of habitat heterogeneity on animal behaviour and reproduction has recently captured serious attention in population and conservation biology. The great tit (Parus major) is a facultative double-brooded species that prefers deciduous forests as breeding habitats. However, it is able to reproduce in managed coniferous forests where nest boxes are provided. During 1999–2002, we measured various reproductive parameters of great tits, including double breeding, in a heterogeneous habitat complex consisting of both deciduous and coniferous forests. Probability of laying a second clutch after the hatch of the first clutch did not differ significantly between habitats. However, clutch size was allocated between two successive breeding attempts more equally in coniferous than in deciduous forests. To our knowledge, this is the first time that such a difference in seasonal breeding patterns between adjacent habitats has been demonstrated in birds. However, the total number of offspring fledged per pair did not differ significantly between habitats. Possible proximate and ultimate causes of the observed habitat differences are discussed. We suggest that habitat-specific allocation of reproductive investment between successive breeding attempts plays an important role in optimizing breeding tactics by facultative multiple-brooded bird species in a heterogeneous environment, potentially serving as a useful mechanism facilitating their adaptation to novel habitats.

Candidate genes for colour and vision exhibit signals of selection across the pied flycatcher (Ficedula hypoleuca) breeding range

The role of natural selection in shaping adaptive trait differentiation in natural populations has long been recognized. Determining its molecular basis, however, remains a challenge. Here, we search for signals of selection in candidate genes for colour and its perception in a passerine bird. Pied flycatcher plumage varies geographically in both its structural and pigment-based properties. Both characteristics appear to be shaped by selection. A single-locus outlier test revealed 2 of 14 loci to show significantly elevated signals of divergence. The first of these, the follistatin gene, is expressed in the developing feather bud and is found in pathways with genes that determine the structure of feathers and may thus be important in generating variation in structural colouration. The second is a gene potentially underlying the ability to detect this variation: SWS1 opsin. These two loci were most differentiated in two Spanish pied flycatcher populations, which are also among the populations that have the highest UV reflectance. The follistatin and SWS1 opsin genes thus provide strong candidates for future investigations on the molecular basis of adaptively significant traits and their co-evolution.

Plumage bacterial load increases during nest-building in a passerine bird

AbstractPlumage bacteria may play an important role in shaping the life histories of birds. However, few studies have examined natural patterns of variation in plumage bacteria. We have previously shown that plumage bacterial load is higher during the pre-laying period than during the brood rearing period in female Great Tits (Parus major). Here, we examined whether the pre-laying bacterial peak in female Great Tits develops during nest-building, where the females come into increased contact with the ground and nest materials, or dates back to an earlier period. Females were captured during three stages of nest-building (nest initiated, nest half ready, and nest completed). The density of plumage bacteria and the species richness of feather-degrading bacterial assemblages were studied using flow cytometry and ribosomal intergenic spacer analysis (RISA), respectively. The density of attached bacteria on feathers increased significantly between nest initiation and nest completion. No effect of nest-building stage on feather-degrading bacterial species richness was found. Our results indicate that the density of attached bacteria in the plumage of free-living birds can change rapidly during nest-building, providing one potential cost of nest-building for individual birds.ZusammenfassungAnstieg in der Bakterienbelastung des Gefieders während des Nestbaus bei einer Singvogelart Gefiederbakterien spielen für Vögel möglicherweise eine bedeutende Rolle der Ausprägung ihrer Lebensgeschichte. Allerdings haben bisher wenige Studien die natürlichen Muster in der Variation von Gefiederbakterien untersucht. Wir haben bereits gezeigt, dass die Bakterienbelastung des Gefieders weiblicher Kohlmeisen (Parus major) in der Zeit vor der Eiablage höher liegt, als während der Jungenaufzucht. Hier haben wir nun untersucht, ob der Bakterien-Peak vor der Legephase bei weiblichen Kohlmeisen während des Nestbaus entsteht, bei dem die Weibchen in erhöhten Kontakt mit dem Boden und mit dem Nestmaterial kommen, oder ob er sich schon zu einer früher Zeit entwickelt. Die Weibchen wurden in drei Phasen des Nestbaus gefangen (Nest angefangen, Nest halb fertig und Nest fertiggestellt). Die Dichte an Gefiederbakterien und die Artenvielfalt Federn abbauender Bakteriengemeinschaften wurden mittels Durchflusszytometrie bzw. einer Analyse der ribosomalen intergenetischen Spacer (RISA) untersucht. Die Dichte anhaftender Bakterien auf den Federn stieg zwischen Nestanfang und -Fertigstellung signifikant an. Auf den Artenreichtum der Federn abbauenden Bakterien hatte die jeweilige Nestbauphase keinen nachweisbaren Einfluss. Unsere Ergebnisse deuten darauf hin, dass sich die Dichte anhaftender Bakterien im Gefieder freilebender Vögel während des Nestbaus schnell ändern kann, was für einzelne Vögel möglicherweise einen Teil der Nestbaukosten verursacht.

Parental provisioning behaviour in Pied Flycatchers Ficedula hypoleuca is well adjusted to local conditions in a mosaic of deciduous and coniferous habitat

Capsule Pied Flycatchers are better able than Great Tits to adjust their feeding behaviour to varying conditions in the same area. Aims Great Tits breeding in a mosaic of deciduous and coniferous forests in the northern temperate region exhibit consistently lower breeding success in their preferred deciduous habitat than in coniferous habitat. This was explained by the unexpectedly poor nestling feeding conditions in deciduous forests of this region. We studied whether the same paradox applies to Pied Flycatchers that occupy the same habitats in the same area. Methods Parental provisioning behaviour was studied using video‐recording and experimental manipulation. Caterpillar abundance and basic breeding parameters were measured in different habitat types. Results Parental provisioning frequency and the proportion of caterpillars in nestling diet was lower, while food objects were on average larger, in coniferous compared with deciduous habitat. However, the total volume of caterpillars and adult Lepidoptera delivered to nestlings did not differ between habitats. In contrast to Great Tits, offspring body parameters in Pied Flycatchers did not differ between habitat types. Conclusions These results demonstrate how the relative suitability of particular habitat types varies between species and is dependent upon geographical location.