One of the ways that primates avoid predators is with the use of alarm calls. If a lemur, monkey, or ape detects a predator, he or she shrieks, warning the rest of the social group. These alarm calls are automatic and reflexive. Just as you can't help but kick you leg when the doctor strikes your knee, the monkey can't help but produce the alarm call. Some species even have different alarm calls to distinguish between aerial predators, like eagles or hawks, and terrestrial predators, like big cats or snakes. To avoid becoming somebody else's dinner, the Sahamalaza sportive lemur (Lepilemur sahamalazensis) eavesdrops on other species' communications.

But the Sahamalaza sportive lemur, one of the world's twenty-five most endangered primates and designated "critically endangered" by the IUCN, has two disadvantages: it is solitary and nocturnal. Since it's solitary, the sportive lemur doesn't have the luxury of relying on alarm calls from nearby group-members. Since it's nocturnal, it is especially vulnerable to predation during the day. When the sun is up, sportive lemurs sleep alone at the entrance of tree holes. They get some protection from the tree, while still staying warm under the sun's heat. That makes them easy picking for their predators: the Madagascar harrier hawk, the fossa (a cat-like carnivore related to the mongoose family), and the Madagascar tree boa. They're also susceptible to poachers hunting for bushmeat.

Lucky for the sportive lemur, though, it shares its habitat with several social species: the crested coua and the Madagascar magbie-robin, both birds, and the blue-eyed black lemur. To see whether the sportive lemur capitalizes on the alarm calls of those species, a group of researchers from the Bristol Zoo, the University of Bristol, and the University of Torino, led by Dr. Melanie Seiler, conducted a playback experiment with 19 Sahamalaza sportive lemurs.

Each sportive lemur was presented with an audio playback of either an alarm call or a song from either bird species. If the lemurs understand the information content of the calls of the coua and magbie-robin, then they should pay attention when played an alarm call, but not when played a regular song. The researchers also played the three different varieties of blue-eyed black lemur alarm call: terrestrial (for ground-based predators), aerial (for air-based predators), and agitation (for general excitement, such as food), as well as a contact call, which lemurs produce while grooming. As with the bird calls, sportive lemurs should display different responses to the three alarm calls as well as the contact call if they can understand the different information conveyed by each type of vocalization.

As the researchers predicted, the Sahamalaza sportive lemurs demonstrated that they understood the different types of information contained in the different types of calls. When played the alarm calls of crested coua and Madagascar magpie-robin, an impressive 94% and 89% of the lemurs changed their behavior from resting to vigilance, respectively. When it came to the bird songs, however, the lemurs all but ignored them. The sportive lemurs also eavesdropped on the calls of the blue-eyed black lemurs. When played the aerial alarm call, 89% switched from resting to vigilance, but the effect was not seen for the terrestrial alarm, agitation, or contact calls.

The lemurs didn't simply look towards the source of the alarm calls, a speaker hidden behind some bushes, which might have occurred if they were just annoyed by the sound. Instead, they looked up and scanned the sky as if they expected an aerial predator, reflecting a nuanced understanding of the calls they had heard.

This pattern shows that the Sahamalaza sportive lemur is clever enough to distinguish between the alarm calls and songs of at least two bird species, as well as between the aerial alarm call and other vocalizations of the blue-eyed black lemur. This is the first scientific evidence of interspecies eavesdropping in a solitary, noctural species: every other known instance of eavesdropping among species has occurred in diurnal, group-living species. They're also the only lemur species known to eavesdrop in this way.

A solitary, nocturnal species like the sportive lemur is especially vulnerable to being killed, either by a predator or by human hunters. The tremendous amount of deforestation occurring on the Sahamalaza peninsula of Madagascar makes the situation even worse. Despite the odds stacked against them, Sahamalaza sportive lemurs survive by paying close attention to the forest chatter going on around them. As usual, evolution works in remarkably efficient ways.

Seiler M., Schwitzer C., Gamba M., Holderied M.W. & Gursky-Doyen S. (2013). Interspecific Semantic Alarm Call Recognition in the Solitary Sahamalaza Sportive Lemur, Lepilemur sahamalazensis, PLoS ONE, 8 (6) e67397. DOI: 10.1371/journal.pone.0067397.t007

Images: Sahamalaza sportive lemur via Wikimedia Commons/Andriaholinirina et al. (2006). Blue-eyed black lemur via Flickr/Donald Ogg. Crested coua via Flickr/Crow 911. Magpie-robin via Flickr/Ross Tsai.

Related:

Eavesdropping Iguanas Use Mockingbird Calls To Survive

More lemurs in The Thoughtful Animal archives:

More Friends Make Lemurs Better Thieves (But What Does It Mean For Brain Evolution?)

Ringtailed Lemurs Look Where You’re Looking

Numerical Cognition and Hidden Grapes

Book Review: Mireya Mayor’s “Pink Boots and a Machete”

Elsewhere:

The Conversation: Lonely lounging lemurs heed warnings of fellow forest creatures