HIGH IN THE Three Sisters mountains of the Cascade Range in central Oregon, researchers had to hike—and then ski—to get to the quiet ephemeral pool. Strange-looking salamanders, and not much else, lived in the water.
“I noticed right away that the [salamander] larvae were really skinny and big-headed,” says Susan Walls, now a research biologist with the United States Geological Survey. When she looked closer, she could see that the heads and jaws of this population of long-toed salamanders were much bigger than normal. It turns out that these larger mouths served a very specific purpose: cannibalism.
In one of the first research papers on this subject featuring salamanders, Walls had described how these larger jaws also held bigger vomerine teeth (which, in this species, are usually just small bumps behind the front row of teeth) that had grown resemble fangs. All the better to eat their brethren with—but why?
The process of "shape shifting" under environmental pressure is called phenotypic plasticity. Long-toed salamanders only do so in the larval stage. Once they're fully grown, like the one pictured here, these changes are no longer possible.
PHOTOGRAPH BY JOEL SARTORE, NATIONAL GEOGRAPHIC PHOTO ARK
As juveniles, before they graduate to living on land, long-toed salamanders can “shape-shift”—their heads and jaws get bigger in proportion to their bodies, and their vomerine teeth become more pronounced. If there’s enough food and water, they won’t grow these features, but if they’re hungry for days and need to get out of their pool quickly (say, during a drier spring or summer), their heads and teeth can grow—and later change back, too. The bigger mouths and fangs help them eat larger prey—including their siblings. This high-protein diet keeps them from starving to death and helps them mature faster so they can get out of the pond before it dries up.
This is an example of phenotypic plasticity—environmentally induced changes to an animal’s appearance—and it’s not just long-toed salamanders that do it. It's evident across various amphibian species and types of animals, too. “There are some insects that have big-headed and small-headed forms, some nematode worms have a cannibal morph with teeth, and there are protists [single-celled creatures] that can produce a cannibal morph in response to crowding,” says David Pfennig, a professor of biology at the University of North Carolina, who has researched this phenomenon in tiger salamanders and spadefoot toads.
Understanding the mechanisms behind phenotypic plasticity is key to using it to help amphibians, which have already declined by 43 percent globally—the highest rate of diversity loss among vertebrates. (Read about how even more species of amphibians are at risk of extinction than we realised.)
Most amphibians are biphasic, meaning they spend their early weeks of life in the water and their adult life on land. It’s during the first part of their life cycle that phenotypic plasticity can occur.
Long-toed salamander larvae, which look a lot like tadpoles, don’t typically eat each other, but they are aggressive: “I saw a lot of bites and snapping when directly observing these animals,” says Erica Wildy, an associate professor of biology at California State University, East Bay, who studied the same subspecies of long-toed salamanders as Walls, as well as others.
A spadefoot toad tadpole normally develops as an omnivore morphs (left). But if it eats large animal prey, such as a shrimp (middle), it'll develop into a distinctive carnivore morph (right), which specialises in feeding on shrimp, other tadpoles, and bigger prey.
PHOTOGRAPH BY DAVID PFENNIG
In the course of her research into how food affected aggression in larval long-toed salamanders, she noted that the isolated mountain salamanders behaved differently from those living in a valley, where food and water was more readily available. She found that the valley salamanders didn’t show as much aggression or any “cannibal morphs,” the name for the big-jawed, pseudo-fanged versions of long-toed salamanders. Wildy’s paper finds that the stress of the nutrient-poor environment is a key factor behind the isolated mountain salamanders’ aggression and cannibalism.
Wildy also noticed that the cannibal morphs seemed to have a faster growth rate compared to those that ate a typical diet of zooplankton. It was probably because they had to grow faster and exit the pool before it dried up, she theorised. A dry pool would mean instant death for a still-larval salamander.
Furthermore, if cannibal morph salamanders move to a more spacious habitat and return to eating their typical diet, they’ll change back to typical morphs, according to Walls.
What kind of pressures can induce such dramatic changes? In the case of the long-toed salamander, it was lack of food and quickly drying seasonal pools. For tiger salamanders, it’s about space—in very crowded conditions, bumping up against each other may trigger the development of cannibal morphs as a way to reduce crowding.
Spadefoot toad tadpoles’ head sizes morph in response to the type of food available. If they happen to eat big prey early in life, some might turn into large-headed morphs, Pfennig says. The normal morph and the big-headed carnivore morph look so different that scientists used to think they were two different species.
Neotropical treefrog tadpoles can develop into different morphs depending on the type of predators nearby. The dragonfly morph (left) develops a colourful tail to distract dragonfiles, whereas the fish morph (right) develops a clear tail that helps them hide from fish.
PHOTOGRAPHS BY JUSTIN TOUCHON
Some morphs are about avoiding predators. Neotropical treefrog tadpoles show distinct morphs in both colour and musculature in response to the types of predators around them.
“If they smell fish in the water, they’ll grow a long, clear tail and have bigger tail muscles,” says Justin Touchon, an assistant professor of biology at Vassar College. It makes it harder for fish to see them and easier for them to swim away quickly.
“But if they smell dragonfly larvae, then they’ll grow a colourful, large tailfin,” Touchon says. This tail will distract the dragonfly so it attacks the more-expendable tail instead of the vulnerable soft body of the tadpole.
Evolution in action?
We don’t know exactly what causes these changes, Touchon says, but gene expression is key. “An animal smells this predator or detects that water is warm, and it turns on some genes that allow it to develop quickly, or suppress other genes.”
He’s currently researching which genes might be responsible for these switches in tree frogs.
If it seems like phenotyptic plasticity is evolution-in-action, well, maybe it is: “Many researchers think that phenotypic plasticity has no impact on evolution since the environmentally induced changes are generally not inherited. Others maintain that plasticity acts to slow down evolution. But another argument suggests that phenotypic plasticity speeds evolution up,” Pfennig says.
Being able to respond quickly to different environmental conditions is an advantage for any species, which has important implications as the climate continues to change. Pfennig’s spadefoot toads in Arizona have ever-shorter time frames to grow from tadpole to toad as the western U.S. sees more droughts and wildfires. Carnivore (or cannibal) morphs may become more common in response—more high-protein food means they’ll be able to grow more quickly into adults, get out of their watery nursery, and breed faster.
“Plasticity should give species a buffer. Having some flexibility can allow species to persist under environmental change,” Touchon says.
Witness the making of a salamander from fertilisation to hatching in this six minute time-lapse.
That could work, but only if the change is something an animal’s plasticity is already prepared for. “An organism’s survival ability depends on where they live, what they are adapted to by past selection, and what climate change is going to do to that place,” says Mary Jane West-Eberhard, senior scientist emerita at the Smithsonian Tropical Research Institute, the Panama-based arm of the Smithsonian Institution focused on tropical ecology.
One example of plasticity helpful for adapting to climate change is that of the threatened frosted flatwoods salamander in Florida. In October 2018, Hurricane Michael pushed saltwater into St. Marks National Wildlife Refuge on the Gulf Coast, where these salamanders breed in freshwater ephemeral pools. After the storm, Susan Walls, who works in the region now, found live salamanders, even at sites inundated with salty seawater.
How could they have survived? “Studies have shown that related animals, like newts, that live in coastal areas, were more tolerant of saltwater conditions than individuals farther upstream. That’s a type of phenotypic plasticity—that they can adapt to more local conditions,” Walls says.
She says she hopes that as scientists learn more about how amphibians can adapt to stressful conditions exacerbated by climate change, humans can use that information to make smarter decisions about protecting them.
Lead Image: An adult long-toed salamander (Ambystoma macrodactylum) photographed in Deschutes County, Oregon. In its larval stage, this species may grow a bigger head and vomerine teeth if food in its pond is scarce.
PHOTOGRAPH BY JOEL SARTORE, NATIONAL GEOGRAPHIC PHOTO ARK