The effect of climate change on avian offspring production: A global meta-analysis.

Climate change affects timing of reproduction in many bird species, but few studies have investigated its influence on annual reproductive output. Here, we assess changes in the annual production of young by female breeders in 201 populations of 104 bird species (N = 745,962 clutches) covering all continents between 1970 and 2019. Overall, average offspring production has declined in recent decades, but considerable differences were found among species and populations. A total of 56.7% of populations showed a declining trend in offspring production (significant in 17.4%), whereas 43.3% exhibited an increase (significant in 10.4%). The results show that climatic changes affect offspring production through compounded effects on ecological and life history traits of species. Migratory and larger-bodied species experienced reduced offspring production with increasing temperatures during the chick-rearing period, whereas smaller-bodied, sedentary species tended to produce more offspring. Likewise, multi-brooded species showed increased breeding success with increasing temperatures, whereas rising temperatures were unrelated to reproductive success in single-brooded species. Our study suggests that rapid declines in size of bird populations reported by many studies from different parts of the world are driven only to a small degree by changes in the production of young.

Improved breeding parameters in the pied flycatcher with reduced pollutant emissions from a copper smelter.

In recent decades, industrial emissions have been reduced in many countries, which provides an opportunity for the recovery of polluted ecosystems. However, our knowledge of the rate and factors facilitating the recovery of local bird populations after pollution abatement is incomplete. Long-term (1989-2021) annual observations on nest-box populations of a passerine bird, Ficedula hypoleuca, were used to analyze temporal dynamics of breeding parameters following a 50-fold reduction of industrial emissions from the Middle Ural copper smelter (MUCS) according to pollution zone, habitat, air temperature, and breeding density. In the heavily polluted (impact) zone (1-2 km of MUCS), egg and fledgling production were strongly impaired compared to the moderately polluted (buffer zone, 4-8 km of MUCS) and unpolluted control zone (16-27 km of MUCS). During the study period, the laying date advanced along with increasing spring air temperatures. The clutch size increased in the impact zone by 26%, in the buffer zone by 10%, and in control by 5%. The number of fledglings increased in the impact zone by 102% and the buffer zone by 17%. In the most recent year (2021), mean laying date, clutch size, fledgling production, and the frequency of nests with unhatched eggs in the impact zone did not reach the control level, whereas the frequency of nests with perished chicks did not differ among zones. Breeding parameters of birds in the impact zone improved slowly, likely due to the slow recovery of habitats. We conclude that bird reproduction may require many decades to recover fully in the heavily polluted zone.

Trophic match/mismatch and reproduction of the pied flycatcher Ficedula hypoleuca in a metal-polluted area.

In polluted areas, birds can suffer from changes in diet composition and inferior food quality. It is unknown if pollution can desynchronize the phenology of birds and their prey, resulting in a mismatch between food demand and availability. For 2 years, we studied seasonal changes in the biomass of leaf-eating invertebrates and the timing of reproduction and breeding success of an insectivorous bird, the pied flycatcher, in an area heavily polluted by the Middle Ural copper smelter and in an unpolluted control area. Seasonal variations in herbivore biomass were relatively synchronous in polluted and unpolluted areas, whereas birds started breeding later in the polluted area. In the year with an earlier spring, the herbivore peak was early and short, resulting in lower food availability for birds feeding nestlings. The greater the mismatch between food demand and availability the higher was the frequency of nests containing perished nestlings and the lower the body mass of fledglings. Our data did not support the hypothesis that the detrimental effect of the trophic mismatch on birds is greater in the polluted area than in the unpolluted one. Nevertheless, delayed breeding in the pied flycatcher in polluted areas suggests a higher probability of mistimed bird reproduction in the years with a short period of food abundance. Thus, the synchrony of phenology of birds and their prey is an important pollution-related factor that should be taken into account when analyzing the effects of pollution on birds.

Thermal effect of the Middle Ural copper smelter (Russia) and growth of birch leaves.

Toxic effects of industrial emissions on vegetation have been extensively studied, and at the same time indirect effects of pollution are less known. In 2011 and 2015, we studied temperature regime and leaf growth for Betula pubescens and B. pendula in deciduous forests near the Middle Ural copper smelter (MUCS). At two polluted sites (1 and 2 km from the smelter) and two unpolluted sites (16 and 27 km), we logged continuously air temperatures during the growing season (May-August) and measured leaves until completion of growth (May-June). Near MUCS, daily mean air temperatures were 0.7-1.0 °C higher with daily temperature range 2.2-2.7 °C greater than at distant sites. Daily air temperature range decreased from spring to midsummer, suggesting that the ability of vegetation to mitigate temperature variations increases with plant biomass, which peaks in midsummer. Growth of birch leaves near MUCS began 4-10 days earlier and completed 3-7 days earlier than far away. Thermal sum over the leaf growth period did not differ between areas in 2011, and in 2015 was lower in the polluted than in the unpolluted area. The earlier leaf growth completion near MUCS can be attributed to higher air temperatures and more rapid accumulation of required thermal sums.

Bird diversity and dissimilarity show contrasting patterns along heavy metal pollution gradients in the Urals, Russia.

The effects of industrial pollution on bird diversity have been widely studied using traditional diversity measures, which assume all species to be equivalent. We compared species richness and Shannon index with distance-based measures of taxonomic, functional, and phylogenetic diversity (the abundance-weighted mean nearest taxon distances), which describe within-community dissimilarity at terminal branches. Analysis of dissimilarity can shed light on the processes underlying community assembly, i.e., environmental filtering decreases dissimilarity whereas competitive exclusion increases it. In the 2-year study near Karabash and Revda copper smelters in Russia, point counts of nesting birds and habitat descriptions were taken at 10 sites (40 plots) along each pollution gradient. The abundance and diversity of birds showed good repeatability in both regions. The total density of birds, number of species per plot, and Shannon diversity decreased at high toxic load in both regions. The taxonomic, functional, and phylogenetic nearest taxon distances showed the same pattern within regions. Species dissimilarity within communities increased with pollution in Karabash (due to loss of functionally similar species), but did not change in Revda (due to mass replacement of forest species by species of open habitats). Pollution-induced changes in bird communities near Karabash were greater due to the stronger deterioration of the forest ecosystems and less favorable natural conditions (more arid climate, lower diversity and vitality of the tree stand and understorey) compared to Revda. This study emphasizes the need for a multi-level approach to the analysis of bird communities using traditional indices of diversity, functional, taxonomic, or phylogenetic distances between species and environmental variables.

Ant (Hymenoptera, Formicidae) diversity along a pollution gradient near the Middle Ural Copper Smelter, Russia.

Ants are considered to be suitable indicators of ecological change and are widely used in land management and environmental monitoring. However, responses of ant communities to industrial pollution are less known so far. We studied pollution-related variations of ant diversity and abundance near the Middle Ural Copper Smelter (Russia) in 2009 and 2013, with pitfall traps set up at 10 sites in Picea obovata and Abies sibirica forest. This study provided evidences for humped pollution-induced dynamics of ant diversity and abundance. Species richness and diversity peaked in the habitat intermediate between slightly damaged and fully destroyed forest ecosystems. The total abundance of ants peaked in the middle of the pollution gradient and was determined mainly by the dominant species Formica aquilonia. The abundance of other species increased towards the smelter, but was less important for total abundance than that of red wood ants. Community dominants changed with increase of exposure; F. aquilonia, a typical species of mature forests, was replaced by species of open habitats, Lasius niger and Myrmica ruginodis. Habitat variables and competition between species seem to affect local ant communities more strongly than pollution exposure. Stand basal area and cover of the field layer were the main determinants of ant diversity and abundance of individual species.

Snail consumption and breeding performance of pied flycatchers (Ficedula hypoleuca) along a pollution gradient in the Middle Urals, Russia.

During the years 1989-91, 1997-2003, and 2005-07, we studied how emissions from the Middle Urals copper smelter affect snail availability and reproduction of free-living pied flycatchers (Ficedula hypoleuca). We counted snail shells dropped in nests and analysed food samples of nestlings. Pied flycatchers brought to nestlings fewer shells in heavily polluted sites compared to background sites, resulting in reduced Ca intake. Species diversity of snails collected by birds decreased with decreasing distance from the pollution source. The pattern was the same both in deciduous and coniferous forests. In sites closest to the smelter, 20-50% of breeding females suffered from Ca deficiency, which resulted in an increased proportion of deserted clutches and clutches with defective eggshells. Number of fledglings per nest decreased in heavily polluted sites, especially in broods with decreased snail supply. This study demonstrated that pollution can cause both direct effect of toxicants to birds and indirect effects via reduced Ca availability.

Large-scale geographical variation in eggshell metal and calcium content in a passerine bird (Ficedula hypoleuca).

Birds have been used as bioindicators of pollution, such as toxic metals. Levels of pollutants in eggs are especially interesting, as developing birds are more sensitive to detrimental effects of pollutants than adults. Only very few studies have monitored intraspecific, large-scale variation in metal pollution across a species' breeding range. We studied large-scale geographic variation in metal levels in the eggs of a small passerine, the pied flycatcher (Ficedula hypoleuca), sampled from 15 populations across Europe. We measured 10 eggshell elements (As, Cd, Cr, Cu, Ni, Pb, Zn, Se, Sr, and Ca) and several shell characteristics (mass, thickness, porosity, and color). We found significant variation among populations in eggshell metal levels for all metals except copper. Eggshell lead, zinc, and chromium levels decreased from central Europe to the north, in line with the gradient in pollution levels over Europe, thus suggesting that eggshell can be used as an indicator of pollution levels. Eggshell lead levels were also correlated with soil lead levels and pH. Most of the metals were not correlated with eggshell characteristics, with the exception of shell mass, or with breeding success, which may suggest that birds can cope well with the current background exposure levels across Europe.

Diet composition as a cause of different contaminant exposure in two sympatric passerines in the Middle Urals, Russia.

Contaminant exposure can vary between species but primary causes of it are often unclear. In order to estimate heavy metal intake of two sympatric passerines - Ficedula hypoleuca Pall. and Parus ater L. - we studied nestling diet and metal concentrations in prey invertebrates, near the Middle Ural copper smelter and in an unpolluted area. Diet of P. ater contained more Cu, Cd and Zn compared to F. hypoleuca and the same amount of Pb. Contribution of different prey taxa to bird metal intake was not equal to their dietary proportion. Proportion of Cu, Zn, Pb and Cd provided to birds by spiders and molluscs, as well as Cd and Pb provided by ants and imagoes Diptera, exceeded their dietary fraction by several times. In contrast, the contribution of Lepidoptera and sawfly larvae to bird metal intake was less than their dietary proportion. Pollution-related changes in the diet modified bird contaminant exposure along with pollutant concentrations in preys.

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.

Geographical variation in egg mass and egg content in a passerine bird.

Reproductive, phenotypic and life-history traits in many animal and plant taxa show geographic variation, indicating spatial variation in selection regimes. Maternal deposition to avian eggs, such as hormones, antibodies and antioxidants, critically affect development of the offspring, with long-lasting effects on the phenotype and fitness. Little is however known about large-scale geographical patterns of variation in maternal deposition to eggs. We studied geographical variation in egg components of a passerine bird, the pied flycatcher (Ficedula hypoleuca), by collecting samples from 16 populations and measuring egg and yolk mass, albumen lysozyme activity, yolk immunoglobulins, yolk androgens and yolk total carotenoids. We found significant variation among populations in most egg components, but ca. 90% of the variation was among individuals within populations. Population however explained 40% of the variation in carotenoid levels. In contrast to our hypothesis, we found geographical trends only in carotenoids, but not in any of the other egg components. Our results thus suggest high within-population variation and leave little scope for local adaptation and genetic differentiation in deposition of different egg components. The role of these maternally-derived resources in evolutionary change should be further investigated.

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 ß-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.

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 Q(ST) (P(ST))-F(ST) 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 (P(ST)) and neutral genetic distances (F(ST)) 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.

Environmental pollution affects genetic diversity in wild bird populations.

Many common environmental pollutants, together with nuclear radiation, are recognized as genotoxic. There is, however, very little information on pollution-related genetic effects on free-living animal populations, especially in terrestrial ecosystems. We investigated whether genetic diversity in two small insectivorous passerines, the great tit (Parus major) and the pied flycatcher (Ficedula hypoleuca), was changed near point sources of heavy metals (two copper smelters) or radioactive isotopes (nuclear material reprocessing plant). We measured concentration of heavy metals and nucleotide diversity in mitochondrial DNA in feather samples taken from nestlings in multiple polluted areas and at control sites. In both species, heavy metal concentrations - especially of arsenic - were increased in feathers collected at smelter sites. The P. major population living near a smelter showed significantly higher nucleotide diversity than a control population in an unpolluted site, suggesting increased mutation rates in a polluted environment. On the contrary, F. hypoleuca showed reduced nucleotide diversity at both smelter sites but increased nucleotide diversity near the source of radioactivity. Our results show that heavy metal pollution and low level nuclear radiation affect the nucleotide diversity in two free-living insectivorous passerines. We suggest that the different response in these two species may be due to their different ability to handle toxic compounds in the body.