On a remote group of islands in the Bahamas, the trees run thick with anoles—lithe, color-changing lizards easily identified by the vibrant fans that adorn the throats of males. Leaping from branch to branch and skittering through the underbrush, these camouflaged reptiles can be tough to spot, let alone catch.
But in the spring of 2015, even the most fleet-footed anoles proved no match for Tyler Kartzinel and his paint-loaded squirt guns.
At the time, Kartzinel, now an ecologist and evolutionary biologist at Brown University, was in the midst of an elaborate experiment. For the previous four years, he and his colleagues had been making regular trips to 16 Bahamian islands to take annual censuses of three local lizard species to see how they interacted over time. One, the brown anole (Anolis sagrei), was a longtime island native. The other two, however, were newcomers introduced by Kartzinel and his team: the closely related, tree-dwelling green anole (Anolis smaragdinus), and the curly-tailed lizard (Leiocephalus carinatus), a known predator of anoles and insects.
Despite their differences, none of the lizards were keen on being snared by human hands. Paint, on the other hand, turned out to be a fast and easy way to tally lizards from afar.
Both brown anoles and curly-tailed lizards frequent the forest floor—and with a squad of hungry predators on the loose, it seemed likely a good portion of the brown anoles would meet their demise. This, in theory, could clear the way for the immigrant green anoles to settle in, thereby boosting island biodiversity.
But as Lizard Paintball 2015 ran its course, Kartzinel and his team began to realize this wouldn’t be the case.
Instead, it was the green anoles who seemed to be declining—and not because they were being eaten. In fact, the curly-tailed lizards didn’t seem to be snacking on either anole. But the fear of being eaten had been enough to drive the brown anoles into the trees, effectively shutting the incoming green anoles out of their would-be habitat. Left with no place to go, the green anoles’ numbers rapidly dwindled, and on one island, they’d even gone extinct.
No war had been waged; no blood had been shed. All the same, a predator had stamped a species out of existence.
Even without directly enacting any physical harm, a predator can cause its prey to alter its very way of living, all by evoking a constant state of fear. The findings of Kartzinel and his colleagues, published today in the journal Nature, suggest this terror can set off a domino effect that extends beyond prey itself, even harming species that predators never encounter—and potentially altering entire ecosystems in the process.
“This is a magnificent study,” says Martha Muñoz, an evolutionary biologist at Virginia Tech who was not involved in the study. “The results really highlight the destructive potential of species introductions...and the fact that we’re just scratching the surface of the ramifications of these actions.”
These findings aren’t the first to suggest that the arrival of a predatory species can sow discord in an existing community. But predators are often billed as a boon to biodiversity: In spots where prey populations compete for the same resources, introduced predators often end up culling members of the more abundant species, thereby leveling the playing field. Without a thorough understanding of ecosystem invasions, ecologists have struggled to forecast their outcomes, which range from benign to catastrophic.
Part of the challenge, Kartzinel says, is that “these events are things we only recognize after they’ve happened. Sometimes the study of evolution is like playing CSI, but with crimes that happened millennia ago.”
And so, to understand how species dynamics play out in real time, Kartzinel and Princeton University’s Robert Pringle led a team of researchers in orchestrating their own ecological crime scene in the Bahamas.
All three lizard species tested are native to the region, but don’t always co-occur on its thousands of islands and cays. Because the isles are tightly packed, creatures occasionally move to and fro, making both invasions and local extinctions fairly commonplace—and setting the ideal stage for an ecological experiment.
The researchers first selected 16 islands that already hosted brown anoles, but not green anoles or curly-tailed lizards. To 12 of these outposts, the team introduced the latter two species in different combinations: Four received a handful of curly-tailed lizards; four got a small group of green anoles; and four were colonized by both. (The final four islands were left undisturbed.)
Over the course of the next six years, the islands followed vastly different trajectories. On islands free of immigrant lizards, the brown anoles flourished, nearly tripling in population size. Even on islands where green anoles entered the picture, the two species managed to peacefully coexist, quickly partitioning the ecosystem in two. While the green anoles kept to the forest canopy, munching on arboreal beetles, their brown cousins foraged for cockroaches on the forest floor.
Where a predator entered the picture, however, this truce shattered—and by early 2017, green anoles had disappeared completely from two of the four triple-booked islands.
This turned out to be the result of a curiously indirect effect. As the more terrestrial of the two anole species, the brown anoles were more likely to run afoul of the ground-dwelling curly-tailed lizards. But the tables were quick to turn: Triggered by curly-tailed terror, the brown anoles began to refuge in the canopies their predators couldn’t reach. By the second year of the experiment, brown anoles were occupying higher perches on tree trunks, and had swapped the dirt-dwelling cockroaches in their diets for leaf-munching beetles.
“There was a clear shift in behavior,” Pringle says. “It’s a bit like, if there’s a shark in the swimming pool, you stay on the deck.”
The simple switch, motivated by fear, had rescued these lizards from a grim fate. (And the curly-tailed lizards seemed content to subsist mostly on insects.) But the brown anoles’ ascension had also taken a dire toll on their chartreuse cousins, who found themselves duking it out for space and resources, and were ultimately ousted. Though the green anole had neither started nor ended its island tenure at any great risk of being eaten, the presence of a predator had still made it the most vulnerable candidate for extinction.
“This really demonstrates that predators have important effects not just by killing prey, but by scaring prey,” says Pacifica Sommers, a community ecologist at the University of Colorado Boulder who was not involved in the study. “And that can still mean life or death.”
The results also cast a sobering light on how much remains unknown about the true repercussions of species invasions—many of which continue to occur, purposefully or not, at the hands of humans.
It’s one thing for researchers to island-hop lizard species within their native region, more or less mimicking what happens naturally. But human have a long history of purposefully introducing plants and animals to places they didn’t exist previously. Though such environmental tinkering may be well-intentioned, it often comes with a bevy of unintended consequences. The addition of Nile perch to Lake Victoria in the 1950s drove hundreds of native cichlid species to near-extinction; a population of cane toads, first introduced nearly a century ago to control beetles ravaging Australia’s sugarcane crop, has since spun out of control.
Through these events and more, humans have, in a way, become the most invasive predators of all, says Simone Des Roches, an ecologist and evolutionary biologist at the University of California, Santa Cruz who was not involved in the study. Mitigating and avoiding these effects, she says, will require broadening our perspectives on just how influential a given species—ourselves included—can truly be in an unfamiliar environment.
“We’re only just beginning to understand what it is we’re doing when we introduce a new species to an ecosystem,” Muñoz says. “When we do so, we’re not just pulling on a single thread. We’re rippling the entire web.”