Esa Lehikoinen

Populations of migratory bird species that did not show a phenological response to climate change are declining

Recent rapid climatic changes are associated with dramatic changes in phenology of plants and animals, with optimal timing of reproduction advancing considerably in the northern hemisphere. However, some species may not have advanced their timing of breeding sufficiently to continue reproducing optimally relative to the occurrence of peak food availability, thus becoming mismatched compared with their food sources. The degree of mismatch may differ among species, and species with greater mismatch may be characterized by declining populations. Here we relate changes in spring migration timing by 100 European bird species since 1960, considered as an index of the phenological response of bird species to recent climate change, to their population trends. Species that declined in the period 1990–2000 did not advance their spring migration, whereas those with stable or increasing populations advanced their migration considerably. On the other hand, population trends during 1970–1990 were predicted by breeding habitat type, northernmost breeding latitude, and winter range (with species of agricultural habitat, breeding at northern latitudes, and wintering in Africa showing an unfavorable conservation status), but not by change in migration timing. The association between population trend in 1990–2000 and change in migration phenology was not confounded by any of the previously identified predictors of population trends in birds, or by similarity in phenotype among taxa due to common descent. Our findings imply that ecological factors affecting population trends can change over time and suggest that ongoing climatic changes will increasingly threaten vulnerable migratory bird species, augmenting their extinction risk.

Climate warming, ecological mismatch at arrival and population decline in migratory birds

Climate is changing at a fast pace, causing widespread, profound consequences for living organisms. Failure to adjust the timing of life-cycle events to climate may jeopardize populations by causing ecological mismatches to the life cycle of other species and abiotic factors. Population declines of some migratory birds breeding in Europe have been suggested to depend on their inability to adjust migration phenology so as to keep track of advancement of spring events at their breeding grounds. In fact, several migrants have advanced their spring arrival date, but whether such advancement has been sufficient to compensate for temporal shift in spring phenophases or, conversely, birds have become ecologically mismatched, is still an unanswered question, with very few exceptions. We used a novel approach based on accumulated winter and spring temperatures (degree-days) as a proxy for timing of spring biological events to test if the progress of spring at arrival to the breeding areas by 117 European migratory bird species has changed over the past five decades. Migrants, and particularly those wintering in sub-Saharan Africa, now arrive at higher degree-days and may have therefore accumulated a ‘thermal delay’, thus possibly becoming increasingly mismatched to spring phenology. Species with greater ‘thermal delay’ have shown larger population decline, and this evidence was not confounded by concomitant ecological factors or by phylogenetic effects. These findings provide general support to the largely untested hypotheses that migratory birds are becoming ecologically mismatched and that failure to respond to climate change can have severe negative impacts on their populations. The novel approach we adopted can be extended to the analysis of ecological consequences of phenological response to climate change by other taxa.

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.

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.

Avian migrants adjust migration in response to environmental conditions en route

The onset of migration in birds is assumed to be primarily under endogenous control in long-distance migrants. Recently, climate changes appear to have been driving a rapid change in breeding area arrival. However, little is known about the climatic factors affecting migratory birds during the migration cycle, or whether recently reported phenological changes are caused by plastic behavioural responses or evolutionary change. Here, we investigate how environmental conditions in the wintering areas as well as en route towards breeding areas affect timing of migration. Using data from 1984 to 2004 covering the entire migration period every year from observatories located in the Middle East and northern Europe, we show that passage of the Sahara Desert is delayed and correlated with improved conditions in the wintering areas. By contrast, migrants travel more rapidly through Europe, and adjust their breeding area arrival time in response to improved environmental conditions en route. Previous studies have reported opposing results from a different migration route through the Mediterranean region (Italy). We argue that the simplest explanation for different phenological patterns at different latitudes and between migratory routes appears to be phenotypic responses to spatial variability in conditions en route.

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.

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 effects on migration phenology may mismatch brood parasitic cuckoos and their hosts

Phenological responses to climate change vary among taxa and across trophic levels. This can lead to a mismatch between the life cycles of ecologically interrelated populations (e.g. predators and prey), with negative consequences for population dynamics of some of the interacting species. Here we provide, to our knowledge, the first evidence that climate change might disrupt the association between the life cycles of the common cuckoo (Cuculus canorus), a migratory brood parasitic bird, and its hosts. We investigated changes in timing of spring arrival of the cuckoo and its hosts throughout Europe over six decades, and found that short-distance, but not long-distance, migratory hosts have advanced their arrival more than the cuckoo. Hence, cuckoos may keep track of phenological changes of long-distance, but not short-distance migrant hosts, with potential consequences for breeding of both cuckoo and hosts. The mismatch to some of the important hosts may contribute to the decline of cuckoo populations and explain some of the observed local changes in parasitism rates of migratory hosts.

Pollution: Recovery of breeding success in wild birds

We have found that the breeding success of two insectivorous forest passerines, the great tit Parus major and the pied flycatcher Ficedula hypoleuca, has markedly improved in the vicinity of a copper-smelting plant during the seven years since it reduced its emissions of heavy metals. Our results demonstrate that reduced pollution loads can positively affect breeding performance of wild bird populations over a relatively short period, even in an area that has suffered decades of heavy-metal pollution.

Urban development from an avian perspective: causes of hooded crow (Corvus corone cornix) urbanisation in two Finnish cities

The hooded crow (Corvus corone cornix) colonised Turku and Helsinki, two cities in southern Finland, in the first half of the 20th century as a breeding species. Their urban population densities, however, remained low for decades, in spite of considerable changes in the urban environment. Since the 1960s, the breeding populations have increased very rapidly in both cities. The possible causes of the early colonisation of cities, the long period of low population density, and the recent rapid population increases are discussed based on environmental history data. The establishment of city parks in the 19th century was probably a prerequisite for initial colonisation, although it cannot alone explain the timing of colonisation. Hooded crow populations did not increase before the 1960s, although biological waste production increased considerably and large landfills were continuously available near both cities. In Turku, the rapid increase of the crow population took place after the availability of biological waste in the main landfill had decreased due to opening of a municipal waste incinerator. Suitable habitats created by urban expansion and a lack of predators in cities during the breeding season may have promoted urbanisation. The main factor promoting urban population growth has probably been decreased persecution in cities since the 1960s. Low levels of persecution in urban areas have facilitated the habituation of crows to humans and traffic, and probably explain the recent colonisation of city centres as breeding habitats.