Tapio Eeva

Large–scale geographical variation confirms that climate change causes birds to lay earlier

Advances in the phenology of organisms are often attributed to climate change, but alternatively, may reflect a publication bias towards advances and may be caused by environmental factors unrelated to climate change. Both factors are investigated using the breeding dates of 25 long–term studied populations of Ficedula flycatchers across Europe. Trends in spring temperature varied markedly between study sites, and across populations the advancement of laying date was stronger in areas where the spring temperatures increased more, giving support to the theory that climate change causally affects breeding date advancement.

The design of artificial nestboxes for the study of secondary hole-nesting birds: a review of methodological inconsistencies and potential biases

Abstract. The widespread use of artificial nestboxes has led to significant advances in our knowledge of the ecology, behaviour and physiology of cavity nesting birds, especially small passerines. Nestboxes have made it easier to perform routine monitoring and experimental manipulation of eggs or nestlings, and also repeatedly to capture, identify and manipulate the parents. However, when comparing results across study sites the use of nestboxes may also introduce a potentially significant confounding variable in the form of differences in nestbox design amongst studies, such as their physical dimensions, placement height, and the way in which they are constructed and maintained. However, the use of nestboxes may also introduce an unconsidered and potentially significant confounding variable due to differences in nestbox design amongst studies, such as their physical dimensions, placement height, and the way in which they are constructed and maintained. Here we review to what extent the characteristics of artificial nestboxes (e.g. size, shape, construction material, colour) are documented in the ‘methods’ sections of publications involving hole-nesting passerine birds using natural or excavated cavities or artificial nestboxes for reproduction and roosting. Despite explicit previous recommendations that authors describe in detail the characteristics of the nestboxes used, we found that the description of nestbox characteristics in most recent publications remains poor and insufficient. We therefore list the types of descriptive data that should be included in the methods sections of relevant manuscripts and justify this by discussing how variation in nestbox characteristics can affect or confound conclusions from nestbox studies. We also propose several recommendations to improve the reliability and usefulness of research based on long-term studies of any secondary hole-nesting species using artificial nestboxes for breeding or roosting.

Growth and mortality of nestling great tits (Parus major) and pied flycatchers (Ficedula hypoleuca) in a heavy metal pollution gradient

We studied nestling growth, growth abnormalities, mortality and breeding success of two hole-nesting passerines, the great tit (Parus major) and the pied fly-catcher (Ficedula hypoleuca), at 14 study sites around a copper smelter complex in Harjavalta, south-west Finland in 1991–1993. The main pollutants in the area are heavy metals and sulphuric oxides. Exposure of birds to heavy metals was shown by measuring their faecal concentrations. Copper, nickel and lead contents of nestling faeces were high near the factory and decreased with distance away from the pollution source. F. hypoleuca nestlings suffered high mortality very close to the factory complex, but did relatively well at all other sites. Breeding success of P. major was below background levels up to 3–4 km from the pollution source and nestlings grew poorly close to the factory. Growth abnormalities of legs and wings in F. hypoleuca nestlings were significantly more common near the factory than farther away. In contrast, F. hypoleuca nestlings grew equally well at all distances. The poor breeding success of F. hypoleuca close to the factory complex is probably related to the high amount of heavy metals in its diet, and low availability of calcium-rich food items may enhance this effect. We suggest that the poor breeding success of P. major is related to habitat changes that have taken place around the factory. The different responses of these two bird species are probably due to their different diet. Our results show convincingly that species-specific differences in response should be carefully considered when planning schemes for air pollution monitoring.

Metal-related oxidative stress in birds

Metals can cause oxidative stress by increasing the formation of reactive oxygen species (ROS), which render antioxidants incapable of defence against growing amounts of free radicals. Metal toxicity is related to their oxidative state and reactivity with other compounds. Our aim is to review the mechanisms on how metals cause oxidative stress and what is known about metal-induced oxidative stress in wildlife. Taking birds as model organisms, we summarize the mechanisms responsible for antioxidant depletion and give a view of how to detect metal-induced oxidative stress in birds by using different biomarkers. The mechanisms producing the harmful effects of oxidative stress are complex with different biomolecular mechanisms associated with ecotoxicological and ecological aspects. The majority of the studies concerning metals and ROS related to oxidative stress have focused on the biomolecular level, but little is known about the effects at the cellular level or at the level of individuals or populations.

Egg shell quality, clutch size and hatching success of the great tit (Parus major) and the pied flycatcher (Ficedula hypoleuca) in an air pollution gradient

Egg shell thickness, egg volume, clutch size and hatching success of Parus major and Ficedula hypoleuca were studied at 14 study sites around a copper smelter complex in Harjavalta, south-west Finland, in 1991–1993. In 1991–1992 unhatched eggs were collected to measure shell quality. F. hypoleuca was more susceptible to pollutants than P. major, the response of which was weaker in all aspects studied. Egg shells of F. hypoleuca were about 17% thinner and eggs were about 8% smaller in volume near the factory than at a distance of 10 km. The clutch size of F. hypoleuca was significantly smaller and hatching success markedly lower at a study site next to the factory complex than at all other sites. In P. major, variation in shell thickness and egg volume was not significantly related to the distance from the pollution source. Clutch size and hatching success of P. major did not significantly differ among study sites, although the trend in hatching success was in the same direction as in F. hypoleuca. Clutches of both species contained less shell material and both species had more nests without eggs near the factory than further away. The surface structure of the eggshells was studied by scanning electron microscope. Especially in F. hypoleuca, the egg shell surface was more rough and porous near the factory. The roles of Ca and heavy metals in shell thinning are discussed.

Pollution-related changes in diets of two insectivorous passerines

Insectivorous birds living in polluted areas are not only exposed to pollutants but they may also be affected by changes in their invertebrate food. The populations of many invertebrate species are affected by environmental pollution and such changes may lead to differences in the diet of insectivorous birds. We examined nestling food quality (invertebrate composition and heavy metal levels) and breeding performance of two cavity-nesting passerines, the Great tit, Parus major, and the pied flycatcher, Ficedula hypoleuca, in an area with long-term heavy metal pollution by a copper smelter. There were no differences in feeding frequencies or the amount of food that parents provided to their nestlings between polluted and unpolluted sites, but food quality in a polluted area differed from that of the control area in both bird species. P. major took more beetles and variable “flying insects” and less caterpillars (of smaller size) and moths in the polluted area as compared to the unpolluted one. F. hypoleuca ate more beetles and larvae and less moths and spiders in the polluted area. Breeding success of P. major was better when the nestling diet contained a large proportion of caterpillars and the relationship was especially strong in the polluted area. On the contrary, F. hypoleuca broods succeeded equally well with variable diets. Our data suggest that a more opportunistic forager, F. hypoleuca, is less vulnerable to a changing invertebrate composition caused by human environmental impacts than a caterpillar specialist, P. major. In a heavy metal polluted area, F. hypoleuca seems to be more sensitive to a decreased amount of Ca rich food items (e.g. snails) while P. major suffers especially from the lack of carotenoid rich caterpillars. Our results emphasize the importance of secondary environmental changes, like food quality, in addition to direct impacts of pollutants.

POLLUTION-RELATED VARIATION IN FOOD SUPPLY AND BREEDING SUCCESS IN TWO HOLE-NESTING PASSERINES

We studied to what extent changes in the breeding performance of two insectivorous passerines, the Pied Flycatcher (Ficedula hypoleuca) and the Great Tit (Parus major) were associated with pollution-induced variation in the biomass of invertebrate prey (spiders and insects on the ground, lepidoptera and sawfly larvae in tree canopies) in an air pollution (copper smelter) gradient. At the nestling time of both species, larvae were scarce in Scotch pine (the dominant tree species) close to the factory complex, peaked in the moderately polluted zone 2–4 km from the factory, and tended to decrease farther away. Both bird species preferred pine, particularly in the moderately polluted zone, where the proportion of larvae in the diet of P. major was high. Ground-living arthropods were scarce near the factory, but among-site variation was high even in the cleanest area. Breeding success of both bird species correlated positively with prey biomass, but only in P. major was food abundance correlated with nestling growth. Also, the productivity of different-sized clutches was affected in P. major, but not in F. hypoleuca. Large F. hypoleuca clutches produced more fledglings than did smaller clutches in all parts of the pollution gradient. For P. major, this was true only in the moderately or slightly polluted parts of the gradient; in the most polluted areas, clutches of 6–11 eggs invariably produced 3–4 fledglings. The stronger impact of food on P. major than on F. hypoleuca probably resulted from a different diet. F. hypoleuca, which forages much from the ground layer, was susceptible to direct effects of pollutants at the egg stage, whereas P. major, a caterpillar specialist, suffered from the shortage of larvae in the late nestling period. Our results indicate that the reduced breeding performance of birds in the polluted area may be due to various reasons; one species may respond directly to toxicity, and the other species to reduced food supply.

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.

Breeding performance of blue tits (Cyanistes caeruleus) and great tits (Parus major) in a heavy metal polluted area

We compared heavy metal levels, calcium levels, breeding parameters and condition of nestling and adult Cyanistes caeruleus and Parus major along a heavy metal pollution gradient. Both species started laying earlier and showed inferior nestling growth and smaller fledging probability in the polluted areas, which are phenologically advanced in spring due to sparse forests. The major inter-specific difference in the responses was that the clutch size and hatching success were decreased in the polluted area in P. major, but not in C. caeruleus. Heavy metal profiles in nestling feces were relatively similar in the two species, though Ni and Pb levels were higher in C. caeruleus than in P. major. However, the latter species showed markedly higher fecal calcium concentrations. Lower calcium levels and higher levels of some heavy metals in C. caeruleus suggest that in Ca-deficient environments this species might be more susceptible to negative pollution effects than P. major.

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.