Climate change ecology
Most organisms are affected by climate: where they occur, how their physiology is organized, or when they breed or migrate. Climate change is thus expected to affect organisms in many possible ways. Long-term data clearly show changes in species ranges or timing of breeding. Some species may profit from these changes, whereas many more are likely to suffer, because their populations are already under pressure through habitat destruction or other human related activities. Little is known how the projected climate change will affect population dynamics, let alone the functioning of entire ecosystems, and the potentially cascading effects must be a concern for society at large.
From a biologists’ perspective, climate change is an interesting experiment, because the process of adaptation to changing environments can be studied in detail. How quickly do species adapt, and how do species differ in speed of adaptation? Are evolutionary changes observed and required or can flexible responses suffice? What are the consequences for population dynamics if a species does adapt insufficiently? And how would this affect the stability of ecosystems? These are the kind of questions our research group is dealing with.
Pied flycatchers as model species
Most of our work is performed on a small insectivorous passerine, the pied flycatcher. This species can be easily studied, because it readily uses artificial nest boxes for breeding. We capture all parents and give them unique rings, as we do with their offspring. By creating such a pedigree we can study the inheritance of important ecological traits, like migration and breeding dates. Knowing whether traits have a genetic basis is important for the study of possible evolutionary responses to climate change. In our study population in SW-Drenthe (NL) we have annually more than 300 pairs breeding in nest boxes, and more than 100 young recruiting as breeders which we ringed locally.
Pied flycatchers can furthermore easily be manipulated during the nestling stage. We can study their diets by using nest box cameras. We can experimentally investigate the direct consequences of hatching early or late in the season by changing the hatching dates of nests. And we even managed to make Dutch pied flycatcher pairs to breed successfully in Sweden under natural conditions by translocating them.
Phenology among trophic levels
In nature one of the most notable effects of climate change is the advance of timing of seasonal events, like flowering of plants and reproduction in animals. At first glance, this seems to be a good response, because when it is warmer organisms can make use of longer growing seasons. However, species often differ in the extent of such a response to climate change, which may cause problems.
Many birds breed in the spring when abundant food is present during a short period. Forest breeding song bird species mostly hatch their chicks when caterpillars are abundant. In the Netherlands, this caterpillar peak lasts for only three to four weeks, after which most caterpillar species pupate and become unavailable to the birds. A proper match between hatching and the caterpillar peak guarantees a high reproductive success.
As a result of climate change caterpillars in the Netherlands and the UK have advanced their peak dates about 20 days between 1985-20101,2. The birds that rely on these caterpillars for chick feeding have responded in diverse ways: in the UK great tits responded to a similar extent with their hatching dates and thus maintained their synchrony. However, in the Netherlands responses differed among trophic levels, and tits and flycatchers increasingly bred too late to fully profit from the caterpillar peak1. Whereas tits and flycatchers did advance their hatching dates, sparrowhawks that rely on abundant passerine fledglings to feed their offspring did not at all advance their hatching dates. The responses to climate change we observe are thus not always sufficient to match the changes in timing of important food sources.
Consequences of an insufficient timing response to climate change?
One consequence of the increasing mismatch between hatching date and the caterpillar peak is that late breeding individuals have increasingly lower reproductive success. This is most likely due to the change in food availability. With the pied flycatchers in the Netherlands we have been measuring chick diets with nest box cameras in different years. In cold springs like 2010 and 2012, both early and late breeders provide their chicks mostly with caterpillars, whereas in warm springs like 2007 and 2011 only the earliest nests get caterpillars, whereas the later nests are raised on a mixture of other insects.
Between 1980-2001 the reproductive advantage of breeding early increased; i.e. later breeders performed increasingly worse relative to early breeders3. Interestingly, this did not lead to a decline in the mean reproductive success of pied flycatchers. Preliminary data do suggest that in recent years selection for early breeding has diminished again, suggesting that the flycatchers are adapting to a certain extent to climate change.
Pied flycatcher populations were affected by the insufficient response in timing to climate change: local populations in the Netherlands that were breeding in rich oak habitats with an early food peak declined towards extinction. In habitats with later caterpillar peaks such a decline was not observed4.
1 Both C et al (2009). J. Anim. Ecol. 78:73-83
2 Charmantier A et al (2008). Science 320:800-803
3 Both C & Visser ME et al (2001). Nature 411:296-298
4 Both C et al. (2006). Nature 441:81-83
Climate change and interspecific interactions
One of the most compelling effects of climate change is on breeding phenology in birds. Many species have advanced their breeding phenology during the last decades, and within species the strongest advances were observed in regions within Europe with the highest temperature changes. Whether these changes are sufficient to match the changes in timing of important food sources is still an open question. In some cases they are, in others they seem to lag behind, and may even result in population declines.
What is often not considered is whether one bird species by changing its phenology, also affects the optimal response of another species that shares the same resource. Interspecific competition may either increase of decrease if one species changes its timing more than the other species. To understand this better, responses of co-occurring populations of competing species should be compared, and their niche overlap measured in circumstances with more and less overlap in breeding time.
We are starting this approach, by studying interactions between different nest box breeding passerines (mostly tits and flycatchers).
Climate change and migration: Being at the right place at the right time
Species may differ in how they adjust to climate change, and one factor that likely constrains rapid adjustment is migratory behavior. Because long-distant migrants winter thousands of kilometers away from their breeding grounds, they likely have difficulties to anticipate on year-to-year changes in the optimal phenology of their breeding grounds.
Pied flycatchers are long-distance migrants. They spend most of their life in West Africa, arrive in April at their European breeding grounds and depart again in early August. This life style makes optimal use of the spring burst of insects in temperate habitats, while retracting to the benign winters of subtropical regions. We study their migratory behavior using geolocation loggers, which gives indications where they winter, when they leave the breeding grounds in the fall, and when they leave Africa in spring. The first results show that these birds take on average 40 days to migrate to the wintering grounds in West Africa, and only 20 days in spring. Since they arrive only shortly before breeding, they have little flexibility to anticipate to the ongoing advance in spring migration, and especially not to the year-to-year variation in spring phenology.
Whereas flycatchers cannot easily adjust with flexibility, we observe that many species of long-distance migrants, including flycatchers, now arrive earlier at their breeding grounds than 20 years ago. How have they managed? Is this a result of ongoing evolutionary change, or is there an unknown mechanism of phenotypic flexibility, that may contribute to this ongoing change over the generations. We study this by building up a pedigree of ringed individuals for which arrival dates are known for many years, so we can look at inheritance of arrival time and its fitness consequences. Furthermore, we experimentally study how ontogeny may affect timing decisions later in life.
Understanding timing of the annual cycle also requires knowledge of ecological conditions at the African wintering sites. Are there important ecological factors that constrain their departure date, either now or in the future with ongoing environmental change? We have been doing some work on wintering pied flycatchers in Ghana, and hope to continue this in the near future. New tracking opportunities will also arise, which may allow a better identification of the environmental conditions that make some individuals to migrate early and others late.
Climate change and dispersal: Searching for a better place to breed
Adaptation to climate change can work at different scales. Individuals may respond flexibly to local changes in ecology and thereby adjust their phenotypes to the changing circumstances. If this is not possible, they may search for another place to breed, where the environmental circumstances fit their phenotype better. Dispersal as process in adjustment of organisms to climate change has not been studied a lot, partly because it is difficult to track individuals while they move to an alternative site.
Long-distance migrants increasingly arrive too late at their breeding grounds, to profit optimally from the short burst of insects available to feed their offspring. They may have difficulties anticipating the advances in spring, as they have limited flexibility while migrating from their distant wintering grounds. A rather easy solution could be to continue migration to the north, until a habitat is reached where the phenology of major prey fits the phenology of the bird. In this way, individual restore the match with the environmental phenology, but may also allow new evolutionary directions if they bring new genotypes on which selection can act.
Dispersal as a way to adapt seems so easy, that it is difficult to understand that many populations seem to have become mismatched with the phenology of their food supply. One reason could be that costs of dispersing to a distant breeding sites may be high: it may be difficult finding a suitable place, and selection pressure may operate there to which the individual is not adapted (local disease strains?). The individual may thus be better adapted to the single timing trait, but got maladapted for other traits that are important in this environment.
Evaluating the importance of dispersal as adaptation to climate change requires estimates of its occurrence and the associated costs and benefits. Using ring-recapture data we could show that pied flycatchers regularly disperse large distances between birth areas in the UK and breeding in the Netherlands1. Whether this happens more in warmer years, and whether especially late individual disperse to the north is yet unknown, but we aim to find out using stable isotope ratios of flycatcher feathers.
The fitness consequences of long-distance dispersal are ideally studied by experimentally translocating individuals to the north and measure their performance. We managed to do so in pied flycatchers. They were caught in The Netherlands, and brought overnight to southern Sweden, where spring phenology is two weeks later. In a warm spring, we expected these birds to be better timed with the local food peak, and possibly have raised more offspring if local adaptation was relatively unimportant. Although we managed to have the birds breeding here, and they also bred considerably earlier than the Swedish birds, we could not demonstrate an advantage. This was likely caused by the experimental year being exceptionally cold, and/or because these birds were locally maladapted2. We hope to continue these experiments in the near future.
1 Both C (2010). Curr. Biol. 20:243-248, doi:10.1016/j.cub.2009.11.0743
2 Knudsen E et al (2011). Biol. Rev. 86:928–946
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