The stemmed oak, the caterpillar and the great tit

The story of the tallow tit begins with the stammering oak. In early spring, the oak buds open and fresh leaves emerge. It is the food for the larvae of the winter moth. In winter, the moth mother lays her eggs on the oak trees. The eggs overwinter and must be hatched at the right time so as not to miss the young leaves. “It will be accurate today,” says Marcel Visser, head of the Animal Ecology group at the Netherlands Institute of Ecology (NIOO-KNAW) in Wageningen. Since 1993, he has been involved in the institute’s research into tallow tit and winter moth. “If the larvae arrive too late, the leaf contains too many tannins (antibodies) and is difficult to digest.” The larvae then have less chance of survival. But too early is not good either: “Then there is no food, and the young larvae die en masse.”

When the larvae are a little bigger, they are perfect food for the baby titmouses. Each spring, the great tit raises a nest of about ten young, mainly by catching larvae of the smaller winter moth. That period of greasy larvae lasts only about three weeks. During that time, each chick with breasts should gain one gram per day. The parents have to catch almost one larva per minute for this. After three weeks, the larvae lower themselves to the ground on a silk thread to pupate and are out of reach of the bird. “The caterpillar peak is not the same every year, because even before climate change, one year was colder than the next,” says Visser. “The timing of the larval peak can vary by two weeks from year to year.”

A titmouse should gain a gram a day, mainly thanks to eating caterpillars.

Signals from nature

The titmouse must therefore be timed well every year when she starts to breed. 22 days pass between the tall tit’s decision to incubate and her eggs hatching. Visser: “So she has to predict when there will be a lot of food, look a month ahead. She does this based on ‘cues’, signals from nature. An important cue is the length of the day, so she knows what season it is. She also uses the spring temperature to fine-tune each year.”

That prediction went well for the tall tit. “It wasn’t perfect, but the top of the brood and larval tip usually coincide quite nicely.” But now there is climate change. Some times of the year heat up more than others. It is precisely the period of the larval peak (late April to early May) that warms up faster than the period when the great tit decides to breed. The result: the signals are no longer correct. “The old rules that the waist tit used no longer apply. As a result, the caterpillar advances twice as fast as the tit. Scientists call this a pheological mismatch: the timing of the life stages (phenology) of a species and its food are no longer synchronized.

Oak forest with nest box of tall tit, and cloths on which larval excrement is collected to get an indication of the number of larvae.

Marcel Visser, NIOO-KNAW.

The mismatch is because the tall tit can only move a little after the first egg has been laid. “She is flexible with regard to the date of the first egg, but the laying and incubation have a fixed duration. If the temperature suddenly rises during that period, there is not much she can do about it. The larvae then grow faster, while breeding takes just as long.”

Nature in motion

The tit is just one example of climate change affecting animals and plants around the world. From reindeer and deer to fish and amphibians, flowers and their pollinators. Migratory birds also have difficulty predicting the rapidly changing climate of their breeding grounds from a distant wintering site. These discrepancies can disrupt ecosystems and threaten their functions for humans. A mismatch between flowers and their pollinators can put pressure on food production; pest insects can escape from their natural enemies and cause damage to agriculture and forestry. It is therefore important to know how nature reacts to climate change and how quickly it happens.

Caterpillar never too early?

That the caterpillar hatches so much earlier is not good news for the caterpillar itself. Visser: “The winter moth is too sensitive to temperature.” Due to the winter moth’s high temperature sensitivity, the eggs hatched earlier and earlier in the spring. So early, in fact, that the oak tree was still in bud. “At the low point in 1995, there was more than ten days between the hatching of the eggs and the emergence of the oak leaf,” says Natalie van Dis. She is a PhD student in Visser’s group and studies the temperature sensitivity of the winter moth. The mismatch led to huge mortality among the larvae. Van Dis saw in an experiment that half of the newly hatched larvae starved after a day without food. But the winter moth was not doomed to starve. The curse became a blessing, explains Visser. “Death is a difficult choice.” Sensitive larvae starve, the less sensitive survive.

Something special happened: the winter moth evolved. With each new generation after 1995, the egg became less temperature sensitive. Visser’s group, including Van Dis, captures the wingless females of the winter moth every five years on the oak trees in November. Each female’s eggs hatch at different temperatures. This gives them an idea of ​​the sensitivity of her offspring for each female butterfly. That sensitivity has diminished over the years. “It is one of the few species that we have demonstrated a rapid evolutionary response to climate change in the wild,” Van Dis said. “Evidence of Adaptation to Climate Change.” This is how the winter butterfly became a success story from a disaster.

Embryo of a winter moth in the egg, photographed under a fluorescent microscope. Over generations, the eggs of the winter moth have become less sensitive to temperature.

Natalie van Dis, NIOO-KNAW.

tit families

Like any species, the great tit can adapt to the warmer climate in two ways: within an individual and from generation to generation. The first is called plasticity, the second evolution. Since 1955, researchers at NIOO-KNAW have monitored breeding pairs of great tit at four locations in the Netherlands (Hoge Veluwe, Oosterhout, Vlieland and Liesbos). With that data, they can draw a picture of the tall tit’s adaptability. “Climate change was not widely accepted in the late 1990s,” Visser recalls. “When it was said that temperatures were going up, we looked in our series of data and suddenly saw that there was a clear trend in temperature and laying date.” The temperature rose, the laying date became earlier.

To find out if temperature really determined the laying date, the researchers conducted an experiment in aviaries with a pair of chicks each. The climate could be set for each aviary. “We gave one group a low temperature, the other a high one. The birds with high temperature started laying earlier, with low temperature later. So it’s not just a correlation in the field, but a causal relationship between temperature and the laying date of the first egg .”

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slow development

The laying date of an individual tallow tit therefore depends on the temperature. By looking at the pedigree of all great tit since 1955, Visser’s group can find out whether this sensitivity is also passed from parents to offspring – the heritability of laying date. The researchers know (the ancestors) parents, brothers and sisters of each individual great tit. “A tall tit lives and breeds for about two years. So we’ve had many generations since 1955, with laying date and temperature for each tit in a year.” If you plot the laying date against the temperature per individual tit in a graph, you get a line with height (early or late layers) and slope (temperature sensitivity) for each tit. The more similar the lineages are, the higher the heritability of the laying date. Laying date was found to be 16 percent heritable (the rest of the variation in laying date is due to other factors). “It’s not much,” Visser concludes.

Together with the number of children per tit, found as breeding birds in later years (fitness), ecologists can calculate the evolutionary response to selection. A strong response would indicate evolution: the population of great tit becomes more sensitive to temperature with each generation. The evolutionary response turns out to be very small for the laying date of the tit. “This means that the development of the laying date is very slow. This is normal in nature, but now the pace of climate change is perhaps a factor of a hundred too fast for the tall tit to keep up.”

Flotmejse comeback

Nevertheless, the great tit is catching up with the caterpillar. Since 2010, the warming of the larval season has stalled, while the period when the great tit picks up its tracks to breed is warming. The tit therefore breeds earlier and earlier, while the larval stage remains the same. In the longer term, however, Visser expects the warming during the larval period to continue. “Then the tallow tit will definitely be behind.”

The catching up of the great tit is therefore short-lived, and this is not due to the bird’s own adaptability. Both the adaptation in the individual and the evolutionary reaction are too slow. That’s bad news. “We see that the number of young people who survive is decreasing every year,” says Visser. Still, he doesn’t think we’ll be getting smaller breasts any time soon. “There is also a density dependence. In good years, the titmice raise more young, in bad years less. But the few titmice that grow up have a better chance of surviving the year compared to a good year when many young grow up. It is like a lottery: if few people buy a ticket, they have a greater chance of winning.” This buffering effect ensures that the number of great tit remains roughly the same during the winter.

“The French tit will definitely start to fall behind,” says ecologist Marcel Visser.

Fred Briene, NIOO-KNAW.

An ordinary bird

The buffer has a limit. In the long term, Visser expects that in bad years, so few young people will grow up that there will be, so to speak, no tall tit “to pick up the prize” (if for the lottery). Then the population will shrink. “But that buffer is a strong effect that will last for a long time.”

You may wonder who mourns a world without big breasts, but the tall tit is not the only bird with this problem. “It’s a common bird that occurs everywhere in the Netherlands,” says Visser. “This effect of a mismatch is true for many bird species.” The winter feed shelf may therefore look quite a bit emptier in the future.

Sources

  • United Nations Environment Program (2022). Borders 2022: Noise, flames and inconsistencies – new environmental problems. Nairobi.
  • Reed, TE, Gienapp, P., Visser, ME (2016). Testing for biases in selection on avian reproductive traits and partitioning direct and indirect selection using quantitative genetic models. Evolution 70-10: 2211-2225.
  • Visser, ME, Lindner, M., Gienapp, P., Long, MC, Jenouvrier S. (2021). Recent natural variability in global warming attenuated phenomenological mismatch and selection of seasonal timing in great tit. Proceedings of the Royal Society of London B 288: 20211337.

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