Aspens in Alaska. Where has the autumn gold gone?

I’ve lived in Fairbanks, AK now for a decade and a half. As a naturalist, I finally feel like I’ve got a decent grasp on the long term changes that occur around my home in the boreal forest. Animals cycle up and down, or erupt in population booms, only to crash in future years. Species like snowshoe hares follow a regular cycle, their populations rising and falling in predictable patterns. Others, such as spruce bud worms, explode in numbers one year, their silky lines dropping by the thousands from the trees and the following summer there will be no sign of them.

And then there are the species, who don’t emulate either strategy. For the past decade or more, aspen leaf miners (Phyllocnisis populiella), a moth, have been abundant in the boreal forest of Alaska’s interior. In late May or early June, the female will lay her eggs on the surface of the fresh aspen leaves. The eggs hatch, and the larvae burrow into the leaf where they proceed to eat their way around in a winding path. Eating only a single cell layer, they don’t kill the leaf, but leave it looking gray or silver.

The damage isn’t good for the aspens, it cuts back on the trees’ ability to photosynthesize and can cause dieback of the living wood above ground. Still, the aspens are tolerant of these herbivores and survive with relative ease. But the miners change the aesthetic of the forest. Aspen stands, during the summer, should look green, but through the last decade’s outbreak, the forests have been weirdly silver-gray. And come autumn, when the aspens should be turning their famous gold, they instead senesce straight to brown, the forest sad and dark.

Most insect eruptions are like the spruce bud worms I mentioned earlier, they explode and disappear. So each spring, when the aspens have turned from green to gray with the infestation of miners I’ve been surprised. Surely the little monsters would have exhausted themselves, but they haven’t, wearing out their welcome like a years-delayed houseguest.

From Doak and Wagner, 2015. This shows the damage caused by leaf miners to the aspens. If you live in Alaska's interior, you are probably familiar with this sight.

From Doak and Wagner, 2015. This shows the damage caused by leaf miners to the aspens. If you live in Alaska’s interior, you are probably familiar with this sight.

In short, the leaf miners have been an annoyance. But why have they lingered so long? Well two researchers from the University of Alaska, Fairbanks have come up with an answer. Pat Doak and her colleague Diane Wagner published a paper in April of this year in the journal Basic and Applied Ecology on this very subject.

Over the course of a decade they monitored the population of aspen leaf miners, conducted experiments into how and and at what densities the larvae began to compete with one another, and looked into how predators of leaf miners influenced the outbreaks. Competition, it turns out, plays the key role the miners’ story.

I needed to dig up an old ecology text to remind myself of the different kinds of competition noted in their paper, so I’d better step back a moment and provide a little review. Competition occurs when resources are limited. The resource, though often food, can also include things like space, mates, habitat, or other aspects important in the life of the species. Competition between two species is called “INTERspecific competition”, while competition between members of the same species is “INTRAspecific competition”. It’s the latter we are concerning ourselves with here.

Within that division, there are a couple further categories: exploitative competition is when the resource is limited but the individuals don’t interact directly with one another as they compete. (Imagine a herd of deer overgrazing a meadow leaving nothing behind for the next passing group. There is no direct interaction between the animals but they impact the amount of resources available to one another). The second major type of intraspecific competition is when individuals interact with one another as they consume resources. This is called “Interference Competition”. Clear examples include two Dall Sheep rams cracking heads as they bicker over an available female, or bears fighting over a prime fishing spot. These animals are actively challenging each other, one will win and one will lose.

As Doak and Wagner found, it’s interference competition that, strangely, has allowed the aspen leaf miners to remain at such a high population density. It took me a few minutes to grasp this, so to explain it, I’m going to take a moment to talk about what these miners need to survive.

Aspen leaves aren’t that big. There isn’t a lot of space or food available and so any given leaf can support, at most, 2 leaf miner larvae. Yet most leaves had more, sometimes many more, miners attempting to establish themselves. As the larvae eat their way through the leaf, they don’t do it in a haphazard way. Instead, they follow the veins of the leaves, which means sooner or later (usually sooner), they are going to come head to head with their neighbors. The outcome ain’t pretty. Basically, when two come into contact, only one comes out of the interaction alive. By the time they’ve killed each other off, at most only two remain.

There are always survivors. That’s the key here. In my overgrazed meadow example, it’s possible that the deer will completely devour the available food leading to extremely high, even 100%, mortality in the population. But with our miners, they are killing one another long before the food runs out, meaning that some members of the population will always survive. And for the last decade, that number has been right about the carrying capacity of the aspens.

But we’re not done. It gets more complicated. I would expect that any high and sustained population like this would lead to a huge increase in predators. Snowshoe hare population explosions lead to population booms in their major predator the Lynx, so why don’t we see the same pattern here? Doak and Wagner asked that question and conducted predator exclusion experiments to find out the answer.

It boils down to this: the more leaf miners there are, the higher the probability that some individuals on each leaf will escape the predators. At low leaf-miner densities the authors found that parasitic wasps (the miner’s main predator) could significantly impact the population because they could wipe out most or all of the individuals on a given leaf. However, when the population of miners was high, the wasps would kill some, but not all of the miners on each leaf. There might end up being less competition between the miner larvae, but there will be no change to the overall survival.

OK, pause and take a breath, because that was getting out of hand.

After wrapping my head around all those details, I still had questions (of course). First, if this interference competition leads to a stable, high population in miners, then why has the eruption gone on only for the last decade and not perpetually? Related to that, for two years (2013, 2014), the aspens didn’t seem to be so sad looking, more green, less silver. Why the apparent drop in leaf miner population and then sudden re-eruption in 2015? I emailed Dr. Doak and asked.

I felt for sure I was going to hear that climate change was the culprit in the outbreak, but I was wrong. “We haven’t found anything to tie the outbreak or its decline to climate changes. People have speculated that poor overwintering conditions or timing of budburst may have driven the [2013] decline, but that does not seem to be the case.”

Rather larval survival seems to be responsible for both the outbreak and the decline in 2013-2014. She couldn’t pinpoint what exactly caused the decline, but hypothesized it might relate to the miner’s main predator. “It is possible that more miners were killed by the feeding of adult parasitoid wasps. It is really hard to detect this because the wasp makes a very small puncture… and drinks [the leaf miner’s] body fluids through these holes – once done these holes have proven impossible for us to detect so we just see a dead miner but not the cause of death.”

Behavioral shifts in the wasps might lead to an increase in predation, “One of these shifts is a sort of threshold effect where [the wasps] may allocate very little vs quite a lot of energy toward adults feeding on hosts [miners]. For the wasps it is a shift from a strategy of feeding little and laying a small number of eggs relatively quickly to a strategy of feeding a lot so that you can mature more eggs over an extended time.”

In other words, the wasps may have seen an opportunity to increase their reproduction, and seized it. But, sadly for the aspens, the possible increased predation doesn’t seem to have continued. Doak went on, “The population in the Interior hit a low in 2013 but immediately started to rebound. Larval survival was less than 1% in 2012 resulting in the population low the following year. Larval survival was a bit higher in 2013 and substantially higher in 2014-2015. And last summer there were again large stands of aspen with heavy mining damage.”

How this will all play out in the future, whether we will have green aspen forests or silver, gold leaves in the fall or brown, is yet to be seen. Dr. Doak tells me that her lab has a proposal under review which, if funded, will allow them to look into the curious population dynamics of leaf miners. I wish her luck!

A few further thoughts:

Like my post a couple of months back on Red-throated Loons, these questions are not just academic. Understanding plant-herbivore-predator interactions shed light not just on this little species of irritating moth, but provides insight into the broader context of the boreal forest. These researchers are seeing changes in behavior in this system that can impact how populations will shift in the future. Right now the aspens seem able to withstand the damage inflicted by the miners, but in their 2013 paper, these same authors do note that there is a significant die-back of above ground tissue in trees grazed on by miners. It’s conceivable that continued impact of the miners will lead to cumulative effects on aspen trees and therefore the boreal forest at large. Since aspens are the usually the first tree species to recolonize a burned forest, I can imagine some rather nightmarish scenarios resulting in low seedling survival. If this were to play out, an understanding of what drives leaf miner populations would be very valuable indeed. 

I say it again, the importance of science extends well beyond the title of the academic paper.

Thanks to Dr. Patricia Doak of the University of Alaska Fairbanks, for answering my questions in such detail!

The paper on which this post is drawn is:
Doak, Patricia and Diane Wagner. 2015. The role of interference competition in a sustained population outbreak of the aspen miner in Alaska. Basic and Applied Ecology 16:434-442.
The second paper I referred to briefly at the end is:
Wagner, Diane and Patricia Doak. 2013. Long-term impact of a leaf miner outbreak on the performance of quaking aspen. Canadian Journal of Forest Research 43:563-569.