Christiaan Both

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.

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.

Repeatability and heritability of exploratory behaviour in great tits from the wild

We investigated whether individual great tits, Parus major, vary consistently in their exploratory behaviour in a novel environment and measured the repeatability and heritability of this trait. Wild birds were caught in their natural habitat, tested in the laboratory in an open field test on the following morning, then released at the capture site. We measured individual consistency of exploratory behaviour for recaptured individuals (repeatability) and estimated the heritability with parent–offspring regressions and sibling analyses. Measures of exploratory behaviour of individuals at repeated captures were consistent in both sexes and study areas (repeatabilities ranged from 0.27 to 0.48). Exploration scores did not differ between the sexes, and were unrelated to age, condition at fledging or condition during measurement. Heritability estimates were 0.22–0.41 (parent–offspring regressions) and 0.37–0.40 (sibling analyses). We conclude that (1) consistent individual variation in open field behaviour exists in individuals from the wild, and (2) this behavioural variation is heritable. This is one of the first studies showing heritable variation in a behavioural trait in animals from the wild, and poses the question of how this variation is maintained under natural conditions.

Natal dispersal and personalities in great tits (Parus major)

Dispersal is a major determinant of the dynamics and genetic structure of populations, and its consequences depend not only on average dispersal rates and distances, but also on the characteristics of dispersing and philopatric individuals. We investigated whether natal dispersal correlated with a predisposed behavioural trait: exploratory behaviour in novel environments. Wild great tits were caught in their natural habitat, tested the following morning in the laboratory using an open field test and released at the capture site. Natal dispersal correlated positively with parental and individual exploratory behaviour, using three independent datasets. First, fast–exploring parents had offspring that dispersed furthest. Second, immigrants were faster explorers than locally born birds. Third, post–fledging movements, comprising a major proportion of the variation in natal dispersal distances, were greater for fast females than for slow females. These findings suggest that parental behaviour influenced offspring natal dispersal either via parental behaviour per se (e.g. via post–fledging care) or by affecting the phenotype of their offspring (e.g. via their genes). Because this personality trait has a genetic basis, our results imply that genotypes differ in their dispersal distances. Therefore, the described patterns have profound consequences for the genetic composition of populations.

Global climate change leads to mistimed avian reproduction

Publisher Summary This chapter discusses the potential consequences of mistiming and identifies a number of ways in which either individual birds or bird populations potentially can adapt to reproductive mistiming. When different components of the food chain shift at different rates, this will lead to mistiming, and it is believed that such mistiming resulting from climate change will be a general phenomenon. The environment at the time avian produce their eggs is, in general much, earlier than the environment when selection will occur on, for instance, synchrony between offspring needs and prey availability. The evolved response mechanisms are appropriate for the range of prevailing conditions, and climate change is a trend that will at first fall within the normal range of temperatures. In the short term, an increase in temperatures may, therefore, allow birds to cope with their existing reaction norms. If these temperatures fall outside the normal range, or if periods in spring differ in their temperature change, the prevailing reaction norms become maladaptive. It is assumed that birds respond to climate change by changes in their laying date solely. However, investigation on pied flycatcher shows that rather than just using laying date as a way to advance hatching date, they use the whole complex of laying date, clutch size and start of incubation. Birds may also adjust other correlated life-history traits as some species show no change in laying date but do respond in whether or not they make a second brood.

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.

Avian population consequences of climate change are most severe for long-distance migrants in seasonal habitats

One consequence of climate change is an increasing mismatch between timing of food requirements and food availability. Such a mismatch is primarily expected in avian long-distance migrants because of their complex annual cycle, and in habitats with a seasonal food peak. Here we show that insectivorous long-distance migrant species in The Netherlands declined strongly (1984–2004) in forests, a habitat characterized by a short spring food peak, but that they did not decline in less seasonal marshes. Also, within generalist long-distance migrant species, populations declined more strongly in forests than in marshes. Forest-inhabiting migrant species arriving latest in spring declined most sharply, probably because their mismatch with the peak in food supply is greatest. Residents and short-distance migrants had non-declining populations in both habitats, suggesting that habitat quality did not deteriorate. Habitat-related differences in trends were most probably caused by climate change because at a European scale, long-distance migrants in forests declined more severely in western Europe, where springs have become considerably warmer, when compared with northern Europe, where temperatures during spring arrival and breeding have increased less. Our results suggest that trophic mismatches may have become a major cause for population declines in long-distance migrants in highly seasonal habitats.

Predicting life-cycle adaptation of migratory birds to global climate change

Analyses of long-term data indicate that human-caused climatic changes are affecting bird phenology in directions consistent with theoretical predictions. Here, we report on recent trends in the timing of spring arrival and egg laying found within a western European Pied Flycatcher Ficedula hypoleuca population. Mean egg laying date has advanced over the past 20 years in this population. The advancement in egg laying date was stronger than the advancement of spring arrival, suggesting that Pied Flycatchers are changing these stages of their annual cycle at different rates. It could be shown that selection for earlier breeding had increased. Hence, the observed adjustment in laying date did not match the advancement of spring. Our findings raise general questions about the adaptability of migratory birds to rapid environmental changes. Adaptive advancement of reproduction in response to increasing spring temperatures and to the concomitant advancement of food supply could be held back, because annual breeding and migration cycles are controlled primarily by endogenous rhythms and photoperiodic cues which do not relate to temperature. Migrants may have several options for arriving earlier on the breeding grounds, including an increase in migration speed, earlier departure from the wintering area or a shortening of migration distance. Changes in migratory behaviour could be accomplished either by phenotypic plasticity or by selection on different genotypes. Although descriptive field data provide compelling evidence for changes in, and possible constraints on, the timing of breeding and migration, their explanatory power in predicting the limits of adaptation remains restricted. We review recent experimental approaches, which explicitly test the relative roles of genetic versus environmental factors in the adaptation of life-cycle timing to global environmental changes.

Flexibility of Timing of Avian Migration to Climate Change Masked by Environmental Constraints En Route

During the past decades, phenology of many organisms has advanced in response to climate change [1]. Earlier arrival of long-distance migrants has been reported frequently [2, 3], but advancements of arrival and breeding were not always sufficient to match phenology at other trophic levels [4]. This has led to increased selection for early breeding [5] and severe population declines [6, 7]. This inadequate response has been explained by an inflexible start of migration, governed by cues unrelated to climate change, such as photoperiod [8]. It has been suggested that evolution at the genetic level is required for a change in photoresponsiveness [9]. Recently, such an evolutionary change in migration timing was suggested [10]. Here I show that timing of spring migration of pied flycatchers (Ficedula hypoleuca) has responded flexibly to climate change. Recovery dates during spring migration in Northern Africa advanced by ten days between 1980 and 2002, which was explained by improving Sahel rainfall and a phenotypic effect of birth date. The lack of advance on the breeding grounds most likely was due to environmental constraints during migration. Adjustment of arrival date in migrants to climate change could thus be rapid, but only if circumstances favorably change for the whole journey.

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.