Climate Change Transforms These Cute Little Birds Into Murderous Brain-Eating Zombies

Although a resident bird species, the great tit, typically breeds two weeks earlier than a migratory species, the pied flycatcher, these birds’ breeding periods now increasingly overlap due to climate change-related factors, leading to serious conflicts over nest cavities that transform cute little birds into vicious brain-eating murderers

by GrrlScientist for Forbes | @GrrlScientist

Great tit (Parus major), in Sweden, winter 2016.
(Credit: Bengt Nyman / CC BY-SA 4.0)

Global warming — or “global weirding” as it is sometimes known — has a lot of strange and unexpected effects upon climate, such as temperature extremes that result in hotter heat waves and colder cold snaps, more frequent droughts, more ferocious flooding, and of course, ocean acidification and sea level rise. But is climate change affecting the annual and seasonal cycles and abundances (phenologies) of plants and animals? Well, yes: researchers are already busily documenting that the frequency, intensity and direction of interactions between living things are being altered by global warming (ref). For example, we’re now seeing that climate change is disrupting both ecosystems and species interactions over time scales ranging from millennia to just a few years’ time by changing the relative abundances and geographic ranges of species, by causing extinctions, and by creating transient and novel communities dominated by generalist species and interactions.

A recently published research paper documents how warming winter and spring temperatures are causing a migratory bird to come into deadly conflicts with a resident bird species (ref) when previously, these two species’s life histories had mostly prevented direct competition between them. Basically, the two species are affected differently by warming temperatures, which now causes them to directly compete for the same limited resource: nest cavities to raise their families in.

How did researchers figure this out?

A team of researchers, led by Jelmer Samplonius, who was a graduate student at the University of Groningen at the time this research was conducted (he now is a Postdoctoral Research Associate at The University of Edinburgh), and his thesis supervisor, ecologist Christiaan Both, a professor at the University of Groningen, studied interactions between a population of European pied flycatchers, Ficedula hypoleuca, and great tits, Parus major, living in the Netherlands between 2007 and 2016.

Adult male European pied flycatcher, Ficedula hypoleuca, in Finland. Adult females look similar, but the black areas are replaced with brown.
(Credit: EstormizCC0)

Pied flycatchers are small black-and-white songbirds that overwinter in western Africa and migrate to Europe in springtime to breed. In contrast, great tits stay on-territory year-round. Both great tits and pied flycatchers nest in tree cavities, but being residents, great tits nest an average of 16.6 days earlier than do the flycatchers in the population that Dr. Samplonius and Professor Both studied. This difference in nesting dates usually prevented the two species from coming into conflict over nest cavities since the fledgling tits were vacating their nest cavities around the same time that flycatchers were beginning to nest. Although fatal competition for nest cavities (a precious and limited resource) has been described previously (i. e.; ref), it wasn’t known whether nor how climate change might affect these interactions. Perhaps warming climate shifts the migratory flycatchers’ springtime arrival to an earlier date so they are suddenly in direct competition with tits for nest cavities? Or might warming temperatures increase winter survival of the resident great tits so there are simply more of them seeking nest cavities?

Resident birds adjust more quickly to warming temperatures than do migratory birds

To test these questions, Dr. Samplonius scored the spring arrival dates for both male and female flycatchers (ref) every day, as well as scoring the dates for when egg-laying was initiated by both flycatchers and tits by checking their nest-boxes every five days to see if they contained eggs. (Songbirds lay one egg per day, so an observer can accurately determine when the birds began nesting by counting their eggs.)

Whilst inspecting nest-boxes, Dr. Samplonius discovered that competition between the flycatchers and the tits for nest cavities was often fatal for the smaller and less aggressive flycatchers: he and his assistants found 86 dead males and 2 dead females during their nest-box checks.

Not so cute now, are they? A great tit with a dead pied flycatcher in its nest.
(Credit: Christiaan Both.)

The dead flycatchers were all discovered in active tit nests. Dr. Samplonius determined that 86 of the flycatchers had been killed by great tits and 2 had been killed by Eurasian blue tits, Cyanistes caeruleus, another resident tit species. All of the dead flycatchers had severe head wounds and usually, their brains had been eaten by the tits.

“Pied flycatchers arrive to breed after great tits have already established their nests,” said Rose Thorogood, a senior research fellow in the Department of Zoology at the University of Cambridge, who was not involved in this study.

“Because time is short, [pied flycatchers] need to establish a territory and find good nesting locations quickly. Visiting the tits’ nests is one way that they can do this — either they can learn about what makes a good nest site in the local area [ref], or they can try to usurp the tits and use the nest for themselves,” Dr. Thorogood explained in email. “This study shows us that tits fight back and kill their visitors.”

Dr. Samplonius found that the tits inflicted a serious mortality rate on male flycatchers in some years, with as many as 8.9% of nesting males being killed in a single year, and with a local annual survival for male flycatchers of just 46% (ref). However, Dr. Samplonius noted that there was large variation amongst years in the number of flycatchers that were killed by tits. Why?

By correlating local temperatures with nest-box killings, Dr. Samplonius found that the resident tits were more responsive to temperature changes than were the migratory flycatchers (Figure 1): great tit laying dates responded to an earlier (February 25 to April 8) and longer (37 days) climate window than pied flycatcher laying dates (April 18 to May 2, only 14 days) and, as you would expect, flycatcher migration arrival dates were unrelated to local temperatures on their breeding grounds.

Figure 1. Differential Phenological Sensitivity to Temperature between Competing Species
Results of sliding window analysis for tit and pied flycatcher phenology in relation to local temperature. Tits adjusted mean egg laying phenology to temperature (2.6 days/C) significantly more than pied flycatchers (0.7 days/C). Flycatcher arrival was unrelated to temperature at the breeding grounds. (doi:10.1016/j.cub.2018.11.063)

Basically, Dr. Samplonius calculated that the sensitivity of great tit laying dates (2.6 days) to warming temperature was about four times higher than pied flycatcher laying dates (0.7 days), showing that climate change differentially affects the phenologies of these two species and the interval between the onset of breeding for each species.

Mild winters and large beech crops lead to higher nest-box occupancy by great tits

“However, like many phenomena in nature, it is not straightforward,” Dr. Thorogood explained in email. “Using their long-term data on phenological changes, the authors show that if the Spring is warmer, then the tits start breeding earlier. This presumably reduces competition and fewer flycatchers die. But, if the winter was warm, then more great tits survive to breed, increasing competition again.”

But was the tits’ increased population solely the result of milder winters, or was another factor, such as food availability, playing a role, too?

To understand the nuances of this relationship, Dr. Samplonius examined the connections between local temperatures and great tit nest-box occupation rates and found that warmer December temperatures (December 6–28) best explained this variation. Did increased food availability also affect this correlation? Dr. Samplonius also considered the beech tree crop from the previous autumn, and found that warmer winter temperatures accompanied by an increased autumnal beech crop were strongly correlated with an increased nest-box occupation rate by great tits the following spring (Figure 2).

Figure 2. Great Tits Occupy More Nest Boxes after Warm Winters
Great tit yearly nest-box occupation in relation to December temperature and beech mast in the previous autumn. Great tits occupied more nest boxes after warmer winters (p < 0.02) and higher beech crops (p = 0.03). (doi:10.1016/j.cub.2018.11.063)

More resident tits means more dead flycatchers in tit nests

Did the date when the flycatchers arrived play a role in their deaths? Yes, although it may surprise you to learn that early-arriving male flycatchers were less likely to be killed by great tits than late-arriving males (Figure 3). Nonetheless, the number of flycatchers killed by great tits was clearly related both to their arrival on the breeding ground as well as to the abundance of great tits, and both of those factors are related to climate.

Figure 3. Synchrony with Great Tits in High-Density Years Was Associated with Higher Mortality
Probability of male pied flycatchers to be killed by a tit in relation to the interval between tit mean laying dates (LD) and flycatcher female arrival in (a) high- and (b) low-density years. The lines were fitted based on GLM outputs, where black represents relatively early flycatcher males and gray late males. (doi:10.1016/j.cub.2018.11.063)

Weirdly, Dr. Samplonius wasn’t able to see any flycatcher population effects as he expected should result from the great tits’ brain-eating zombie festival, so he and Professor Both created a model to test the “dead or alive” pattern that Dr. Samplonius identified versus the overall density of tits, against a number of variables, particularly the overall density of flycatchers.

Dr. Samplonius and Professor Both’s model showed that male flycatchers were most likely to be killed when (1) female flycatchers arrived at the same time that great tits were laying eggs and when (2) the overall density of great tits was high. So in short, their model showed that female flycatcher arrival date was a better predictor of male mortality than male flycatcher arrival date because competition for nest-boxes intensifies after the females show up.

But there is a subtle wrinkle in these data: Dr. Samplonius and Professor Both’s model revealed that some male flycatchers were more likely to be killed than others: they found that late-arriving male flycatchers (who are least likely to breed) were most likely to be killed by great tits, whereas early-arriving males (who are most likely to breed) were also most likely to survive. This indicates that flycatchers are somewhat protected against the most immediate negative effects of this deadly competition over real estate since breeding males are least affected. But as more late-arriving males are killed, this “buffer group” will dwindle, until the entire flycatcher population will feel its consequences.

These findings suggest that climate driven interactions could affect the survival of two competing species more strongly than even the availability and abundance of food (ref).

This elegant study underscores the value of long-term field studies for understanding the effects of climate change

“This study is a fantastic example of how we can use carefully collected long-term field data to understand a puzzling natural history observation,” Dr. Thorogood said in email.

“This is a fascinating study that shows climate change disrupting interactions between different species in an ecosystem: changes in the timing of breeding reduce fatal interactions between competitors,” agreed evolutionary ecologist Loeske Kruuk, a professor at the Australian National University, who was not involved in this study.

Graphical Abstract: Resident birds adjust more quickly to climate warming than do migratory birds. Jelmer M. Samplonius and Christiaan Both (2018). Climate Change May Affect Fatal Competition between Two Bird Species, Current Biology, published online on 10 January 2019 ahead of print | doi:10.1016/j.cub.2018.11.063

“Long-term studies of tits have provided some of the best evidence we have for what is known as adaptive phenotypic plasticity [ref],” Dr. Thorogood elaborated in email. “As spring temperatures warm (or cool), great tits can adjust the timing of when they breed to maximise the chance that there will be plentiful food when rearing their young. This study is fascinating as it goes a step further to show that this plasticity has consequences for how competing species interact.”

As always, long-term field studies are essential for better understanding how climate change affects wildlife.

“The work is rare in containing detailed data on two co-existing wild bird species, and a neat illustration of the value of long-term detailed monitoring of wild animal populations,” Professor Kruuk pointed out in email.

This study shows that resident species have the advantage because they are more responsive to temperature changes triggered by climate change, whereas migratory species are not. As a result, migratory species (which include many of our common and beloved “garden” birds) will suffer greater competition from residents, who will become more abundant as winters become milder, thus allowing them to outcompete migrants seeking food and nest sites even as spring begins earlier. But are these findings applicable only to competitive interactions between resident and migratory species, or might they be generally relevant? If so, how?

“It also provides important evidence for yet another way in which climate change is affecting the natural world,” Professor Kruuk stated in email.

Future studies that manipulate great tit abundances and availability of nest sites could reveal the limits of these effects upon this system, and could also provide information that could be generalized to other systems as well.

“We usually think of cavity nests as being a limited resource, which birds need to fight for,” Dr. Thorogood explained in email. “However, just like in this study, when we provide nest boxes this changes the availability of nest sites. It would be interesting to see if altering the resource that the birds are competing for experimentally would influence the interplay between climate and killing that the research team identified here.”

Source:

Jelmer M. Samplonius and Christiaan Both (2018). Climate Change May Affect Fatal Competition between Two Bird Species, Current Biology, published online on 10 January 2019 ahead of print | doi:10.1016/j.cub.2018.11.063


Originally published at Forbes on 29 January 2019.