Next to lions, we are elephants’ biggest predators. Ivory poaching looms large in the public consciousness, but many elephants are also killed during clashes with humans over water sources, grazing land, and family farms. As the human population grows and continues to encroach on elephant habitats, these skirmishes will only increase in number and intensity.

Because human-elephant conflicts are on the rise, researchers are putting new emphasis on studies of how elephants respond and react to threats. We already know that elephants are relatively street-smart when it comes to humans: they prefer to raid crops on dark nights when they can't be seen and also tend to hustle when travelling through unprotected areas. But recent research is finding that elephants’ cognitive skills are even more sophisticated and flexible than scientists previously thought, raising questions about how successfully they can co-exist and potentially co-evolve with humans.

Different dangers, different calls

One of the biggest advantages to living in groups is that more eyes means heightened vigilance. Some social mammals use different types of alarm calls to warn others of specific threats, varying frequency, pitch, or duration to identify the danger at hand. Other group members can use this information to respond properly. If an eagle is swooping down into the branches, don’t climb a tree, and if there’s a hungry snake below, be sure not to drop to the ground to flee.

But this ability, called referential or representational signaling, is a relatively advanced cognitive task. In some ways, it’s similar to language, since it involves using distinctive vocalizations like names to refer to different objects or concepts. Additionally, it only works if an entire group shares the same vocalizations and understands what each refers to. Primates like vervet monkeys are most famous for this ability, but other social animals like chickens also seem to use it as well.

In many ways, elephants are likely candidates for representational signaling. These long-lived creatures are highly social, relying on their close-knit relationships with other group members for food, water, and protection. They also have rich vocal repertoires full of rumbles, trumpets, and roars.

New research in PLoS presents strong evidence that African elephants refer to different threats with specific alarm calls. An international group of researchers recorded wild elephants’ vocalizations in response to humans and bees, finding that the alarm rumbles elicited by these two types of danger had very different acoustic structures and characteristics. Call rates and frequencies were higher in response to human voices than bees, perhaps reflecting a greater urgency.

When the researchers played these recorded vocalizations back to other elephants, they found that these elephants responded differently to bee-induced and human-induced alarm rumbles. While elephants retreated in response to both types of calls, they also shook their heads vigorously when hearing bee-induced calls, a behavior that researchers see regularly when elephants are actually being attacked by bees. There was no head-shaking in response to vocalizations elicited by human voices.

Although it’s possible that these vocalizations are simply byproducts of a flight response, physiological and behavioral studies back up the researchers’ suggestion that elephants are actively manipulating their vocal tracts to produce these calls. In either case, it does seem clear that other elephants recognize and use information from these vocalizations to inform their own behavior, which is no small cognitive feat in itself.

It’s all in the voice

As scientists look deeper into elephants’ responses to danger, they are finding that there’s even more nuance in how these animals identify and react to specific human threats.

Elephants frequently come into contact with two local tribes in Amboseli National Park: the Kamba, an agricultural group that poses little threat, and the Maasai, who frequently clash with elephants over land and water thanks to their nomadic herding lifestyle. An earlier study showed that elephants here can discriminate between the clothes worn by these two groups via color and scent, but a new paper in PNAS finds that they are capable of even more subtlety when it comes to auditory information. Elephants can distinguish between different subgroups of humans based on vocal cues, using them to assess how much danger a human poses.

The researchers played Maasai and Kamba voices to 47 different family groups of elephants in Amboseli. The playbacks were prerecorded; each said “Look, look over there, a group of elephants is coming” in the speaker’s native tongue. There were several different recordings in each language to ensure that the results weren’t due to eccentricities of a single recorded voice.

Elephants reacted much more strongly to the voices of Maasai men than Kamba men, bunching together defensively and waving their trunks to sniff the air and better localize the threat. It’s not clear whether the elephants can distinguish between the two tribes’ different languages or are simply relying on other vocal cues, but the implication is clear: elephants know who is more dangerous.

But the elephants’ remarkable cognitive abilities don’t end there—within a group, they know who to watch out for. Men pose the greatest danger to elephants because they are usually the ones bearing the spear and the intent to kill. Elephants engaged in significantly more defensive behavior when the researchers played male Maasai voices than female Maasai voices, bunching together, sniffing, and retreating much more often in the presence of male voices. Unexpectedly, the result held up even when the researchers resynthesized the male recordings to match the female speakers’ pitch and frequency, suggesting that elephants may use different cues than we commonly do to distinguish between the sexes.

Adaptively, it makes sense for elephants to react in different ways to these different subgroups. Not retreating in the presence of a male Maasai out for blood is a fatal mistake, but fleeing into the bush every time a Maasai woman or Kamba man is in the area is a costly waste of time and energy.

These two studies demonstrate the sophistication of elephants’ cognitive abilities, at least when it comes to threat detection. The neural architecture required to distinguish between different types of threats has probably been selected across an evolutionary time scale, but there is also a surprising amount of flexibility and learning at work as well. Elephants are likely using both social learning and their own experiences to inform how they respond to new and changing threats.

In some ways, this flexibility—which scientists refer to as “plasticity”—is promising because it suggests that elephants are able to cope with a changing landscape and its inhabitants. However, encroachment and human-wildlife conflict are likely happening too quickly and at too large a scale for elephants to keep up. Elephants and other long-lived mammals like dolphins and primates are disproportionately affected by human disturbance due to small litters, slow development, and large home ranges. So although these big charismatic species are the most likely to have highly developed cognitive skills and abilities, they are also the ones that are most likely to disappear if humans don't step in and help.

PLoS, 2014. DOI: 10.1371/journal.pone.0089403 and PNAS, 2014. DOI: 10.1073/pnas.1321543111 (About DOIs).