The metapopulation study system

Tvaerminne archipelago

The Skerry islands of Tvaerminne archipelago, with the field station (Picture: Jouko Pokki).

This project arose out of the idea to conduct field work in a system with replicated populations. The small rock pools on the Skerry islands of the Baltic Sea allow us to study processes on the population level, and at the same time to study the ecological and evolutionary dynamics of these populations on the metapopulation level.

The rock pools on the Skerry islands of the Baltic Sea harbor freshwater communities, often dominated by Daphnia. We study the ecology and evolution of these Daphnia and their parasites, epibionts and microbiota. The research of this longterm project addresses aspects of local adaptation, metapopulation and metacommunity dynamics (we have more than 30 years of data for more than 500 rock pools), inbreeding, parasitism, and genetic population structure. The slide show gives a short introduction to the environment and the field station in south-western Finland.

Slideshow about the field site in Finland.

Background and the system

Early-on during our research with host-parasite interactions it became clear that we needed a system where we could do experimental work under field conditions. Working with Daphnia in the field seemed hopeless, as most of Daphnia field work at this time was simply taking samples and work through them in the lab. Janne Bengtsson from Uppsala told me about his rock pool study system on the Baltic Coast of Sweden. Along the coast one can find Daphnia populations in small rainwater pools. The population sizes are big enough to talk about real populations and they are easy to study. Our first study was conducted on the Swedish coast, but later we moved to Finland, where we found a perfect research station to conduct our work.

Tvaerminne Zoological station is situated on the Golf of Finland, with many small Skerry islands located close to the station. There are thousands of rock pools on these islands, about 30% of which have Daphnia populations. The pools are inhabited by diverse invertebrates, among them D. magna, D. pulex and D. longispina. Daphnia reproduce mostly asexually but may reproduce sexually, resulting in resting stages for dispersal among pools and to endure the harsh winter conditions and the frequent summer droughts. Average pool volume is about 300 liters, but individual pool volumes range by more than 4 orders of magnitude.

The dynamics of Daphnia in Baltic rock pools have been studied intensively, and much is known about local extinction and colonization. Instrumental for our research was V. Ilmari Pajunen and his wife Irmeli, who worked on the Daphnia rock pool communities already since 1982. Since 1998 we work together. Part of this work involves the assessment of presence/absence of the three Daphnia species in more than 500 rock pools twice a year continuously since 1982. Since 2007 we also record the Daphnia parasites. Besides these we have many metadata for every pool in the study region. This dataset is one of the biggest meta-community datasets in the world.

The Daphnia populations in the rock pools are very dynamic across the years. For example, on average of 17% of pools are occupied by D. magna; 16% of the occupied pools go extinct per year, but re-colonization approximately balances this loss in the long run. Factors that influence Daphnia habitat characteristics in this metapopulation, but also in other Daphnia metapopulation in Europe and America, include interspecific competition, the presence of parasites and predators, isolation in space, salinity, pH, organic matter and pool size. Many of these factors are correlated with each other, making it difficult to determine which factors play a causal role in shaping the distribution of Daphnia.

Over the years we used the Daphnia rock pool system to test hypothesis and answer questions relating to host-parasite interactions, epidemiology, inbreeding and genetic diversity. We also investigated the system itself, aiming to understand the processes at work in shaping phenotypic diversity in the metapopulation context.

Rock pools are constantly changing

The freshwater rock pools are inherently unstable. On the Skerry islands of the Baltic Sea they can only exist in a belt between the shore line and the plant dominated interior of the islands. A pool protected from the sea would quickly be invaded by the roots of perennial plants, which drastically increase evaporation, or would accumulate organic matter eventually turning the pool into a bog. The width of the rocky belt in which freshwater rock pool habitats are found in these islands ranges from between about 0.5 to 10 m above sea level, but may be up to 80 m wide, depending on the exposure and the slope of the rocky shore. The Skerry islands of the Finish archipelago are in an area of post-glacial uplifting, which, in southwestern Finland, occurs at about 3-5 mm per year. Therefore pools are decreasingly influenced by the sea as they age (lifted out of the sea) and increasingly influenced by terrestrial plants. With 4 mm uplifting per year, this succession takes between 100 and 2500 years, depending on the vertical width of the belt with freshwater rock pools. Recently, however, climate change induced increases in sea level have been about 2-3 mm per year, which partially compensates for the effect of tectonic uplifting and will extend the time span during which rock pools can form freshwater habitats. On the other hand, climate change has also led to dryer and warmer summers in southwestern Finland, which creates more frequent drying of rock pools and their sediments. As a result, the wind-exposed resting eggs of D. magna are more efficiently dispersed and the D. magna metapopulation becomes more dynamic, with more recorded extinctions and re-colonization events per year.

Sea eagle

A white tailed sea eagle followed by a herig gull (picture by David Duneau).

The interplay of the sea and terrestrial plants strongly influences the pH and calcium of the pools. Plant invasion causes a drop in pH (because of humic acids), as does the runoff of water with low pH from bog-like pools above the shore after strong rainfalls or melting snow. On the other hand, calcium arrives at pools with seawater waves and spray. Both factors are strongly affected by weather conditions (e.g. rain, wind, snow melt, evaporation, etc.), are highly dynamic and seasonal, and cause changes in water quality in the short term as seen in our time series of these variables. Eider droppings, which contain large amounts of crushed mussel shells, are frequently found around the pools. They have a buffering effect on these dynamics. These droppings strongly elevate calcium and pH of the pool water. Pools without eider droppings are mostly unsuitable for D. magna, making eider ducks an ecosystem engineer for the D. magna metapopulation, which needs a pH above 6.5.

The impact of eider ducks is, however, not only variable across islands but may also vary across time. Eider ducks change their nesting and roosting places from year to year. During nesting season, they seek cover on forested islands, while later in the season they are more frequently observed on more exposed islands. Terrestrial predators such as fox and mink threaten ducks in and close to the forest, while avian predators such as the sea eagle and eagle owl threaten them more on the open islands. Eider ducks may change their roosting sites in response to these changing dominant predators. Mink invaded southwestern Finland only during the last century, and bird predators went through severe population crashes in the last 100 years. For example, in the last 15 years, the sea eagle (Haliaeetus albicilla) population recovered dramatically from near extinction in our study area, which caused a strong increase in predation on adult eider ducks and possibly an associated change in social behavior. A speculative chain of events is that humans influence the sea eagle population, which influences the eider duck distribution, which influences rock pool water chemistry, which ultimately influences D. magna distribution.

Do metapopulations evolve differently?

A key interest of us is the question how a metapopulation evolves and if this differens from our picture of evolution in conventional populations. For this we use breeding genetics, population genetics and genomic tools. Early on it became clear that the Daphnia populations in the rock pools are characterized by low genetic diversity, caused by severe founder effects during colorization of empty rock pools. Inbreeding and hybrid vigor of immigrants are a consequences. Genomic data show that this also leads to the accumulation of deleterious mutations, which may go locally to fixation during founder events of single colonizers. All in all, the signs we see clearly point out that the Daphnia metapopulation evolve differently from Daphnia population in central Europe, which are more stable and genetically more diverse.