In the mid-1600s, green monkeys from Africa were introduced to the West Indies island of Barbados. Despite living a predator-free life for centuries, the Barbados population still responds to an ancestral alarm call that means, roughly translated, “Run up a tree or a leopard will eat you!”

Life-Saving Alarms

One of the primary benefits of group living is that it helps animals avoid becoming dinner for hungry predators. Many species increase their chances of survival by utilizing so-called “alarm calls,” which serve to warn other group members of imminent danger. For some animals, such as vervet monkeys (Chloroecbus pygerythrus), the alarm system is quite complex.


These Africa natives have a specific call for different types of predators, and each call elicits a specific reaction from group members. So when an individual gives a sharp bark, it communicates that a leopard is around, causing group members to climb trees to avoid the big cats, which tend to attack vervets on the ground. A double-syllable cough, on the other hand, signifies that an avian predator — a crowned eagle, for example — has been spotted and that everyone needs to dive into a bush to hide. And when a vervet monkey sees a snake, it produces a low-frequency, monotone vocalization called a “soft chutter” — other monkeys in the area will stand on two feet, look down to find the snake and then mob the serpent.

Interestingly, only males of the species produce these varied alarm calls. Females have a high-pitched chirp that they use in all predator situations, though scientists aren’t sure why. “My best guess is that because females are going to be in close contact with infants, they are, in a sense, more vulnerable to predators,” said Melissa Burns-Cusato, a behavioral neuroscientist at Centre College in Kentucky. “High-pitched noises can be harder to track than lower frequency sounds, so this may be an adaptation to make females more difficult for predators to locate.”


A lingering question for vervet monkeys and other species is how their anti-predator behaviors spread among group members and remain in use over time. Last year, research on Stewart Island robins showed that the birds lose their fear of rats if they’re in a rat-free environment for just one generation, suggesting that their ability to recognize predators and react appropriately is based on experience and learning. But some research suggests that the recognition of predators, production of alarms and responses to alarm calls have a genetic basis, or are even mediated by both genetic and experiential mechanisms.

For vervet monkeys, the evidence had long pointed to an experiential basis for their anti-predator behavior. “Early studies suggested learning rather than genes because infants and juveniles tend to make errors in identifying predators, or they’ll make a call in response to a non-threatening animal,” Burns-Cusato told io9. “But when they get older, those mistakes are very rare, so the alarm call is being refined with experience.”


If this idea is correct, then the monkeys’ anti-predator behaviors should quickly decay if they’re no longer in the presence of their enemies — just like what happened with the Stewart Island robins. But testing this in the wild is difficult because of the lack of predator-free populations, so Burns-Cusato and her colleagues turned to green monkeys (Chlorocebus sabaeus) for some answers.

These primates were once thought to be a subspecies of vervet monkeys, and only within the last 12 years have green monkeys gained recognition as a unique species, Burns-Cusato said. They are still believed to be closely related to vervet monkeys and even share the same anti-predator behaviors as vervets in their home range in Africa. But is the same true for the green monkey populations on Barbados, which haven’t had to deal with their ancient predators for hundreds of years?


Genes or Experience?

To find out, the researchers recorded leopard calls and snake calls from adult male green monkeys in West Africa. They then tested the calls on a group of green monkeys in the Barbados Wildlife Reserve.


When the team played the leopard alarm calls (audio above), almost all of the monkeys instantly climbed up trees. Only three monkeys — a juvenile, a pregnant female and her infant — didn’t climb a tree, and instead hid under a bush.

Oddly, the snake alarm call didn’t elicit any noticeable reaction from the green monkeys. It’s not likely that the primates would recognize the ancestral leopard call but not the snake call, so something else must be going on.

“They didn't really do much of anything, and that could be because they need to see the individual in the bipedal stance, in conjunction with the chutter,” Burns-Cusato explained. “It might not be enough to just have the chutter.”


Indeed, it seems that the monkeys still recognize the danger of snakes. In a follow-up experiment, the scientists placed a rubber snake and a black nylon rope in the green monkeys’ territory. While the primates eagerly picked up the rope and smelled it, they were very wary of the rubber snake, and would only approach it cautiously and stand bipedally, but never get close enough to touch it.

Based on the results, the researchers don’t think the green monkeys’ alarm call system is something that is purely learned, given that the Barbados population still knows what to do in response to the leopard call despite not seeing the big cats since the 1600s. Instead, the primates’ behavior may be a combination of genetic and experiential influences — that is, they have a genetic predisposition to respond to the alarm call, but their experiences tell them what threat they’re actually responding to.


What this implies is that the sharp bark may never have really communicated “run up a tree or a leopard will eat you” — it may have only meant “run up a tree.” While the African populations associate that alarm call with leopards, the Barbados green monkeys may associate it with some other threatening stimulus, though what that danger may be is anyone’s guess (their only real predators are the people of Barbados, who in the past have culled the animals to slow the their population expansion). Adding another layer to the mystery: After 400 hours of observations, the researchers never once heard the monkeys use the leopard alarm call in their natural setting.

For now, the researchers are interested in testing if the Barbados green monkeys recognize their ancient avian alarm call. They are also trying to see if the primates have an inherent visual recognition of leopards, as they seem to have with snakes.


In a pilot experiment, the team found that the monkeys actually avoided images of leopards, but not of waterbucks; another pilot experiment showed the monkeys produce more leopard alarm calls (barks) in response to the leopard images, compared with images of waterbucks. These two experiments still need to be confirmed with further tests, Burns-Cusato said.

Check out the study in the journal Behavioral Processes.

Top image via Tonyingesson/Wikimedia Commons. Inset images via Bjørn Christian Tørrissen/Wikimedia Commons, paulcook2809/Flickr. Audio courtesy of Tabitha Price (Georg-August-Universitat Göttingen).