Why aren't these lemurs singing in harmony?

These lemurs choose not to sing well together, according to new research.

Photo of an indri (Indri indri) lemur, the only species of lemurs that sing in groups as a form of communication.

Courtesy of Giovanna Bonadonna/University of Turin

June 15, 2016

Rebellious teenagers try to dissociate from their parental units every chance they get. And it seems to be no different when that antsy youth is a singing lemur.

Indri indri, the only lemur species that sings, lives in small family groups in the dense Madagascan forest. These groups of animals use their howling voices to form a raucous sort of choir many times each day.

The primate parents sing largely in concert with each other, with their voices overlapping. But the older offspring often punctuate these songs with their own individual vocalizations, avoiding overlapping, according to a new study published Tuesday in the journal Frontiers in Neuroscience.

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"We have this new evidence that overlapping during the song is not something that happens randomly," study lead author Marco Gamba a primatologist at the University of Turin in Italy tells The Christian Science Monitor in an interview. Instead, the lemurs actively try to, or not to, overlap their voices in song.

So why are they singing in these patterns?

Indris live in small social groups formed of a monogamous reproductive pair and their offspring. Each family group has a territory over which it presides. So the lemur choirs, which can be heard from about 1.25 miles away, serve as a sort of "no trespassing" warning.

"The pair wants to overlap because they probably want to tell the others, 'Hey, we are a strong group,' " and 'Keep away,' by amplifying their voices, Dr. Gamba explains. 

It's a bit like a primate version of the play "West Side Story," with gangs of indris singing to intimidate others in place of the synchronized dance-offs between the Sharks and the Jets. The turf war can get violent, but only in rare cases when the lemurs' vocal sparring does not prevail.

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But, like Tony and Maria, the juvenile indris have different priorities.

"The juveniles that are more or less ready to leave the group and start their own reproductive pair probably want to avoid overlapping to say, 'Hey! I can mate, I can create a new group,' " to attract potential mates, Gamba says.

The lemurs kick off their chorus with aggressive roars before they break into song. Then, the indri choir sings in phrases made up of two to six notes that descend in pitch, like air escaping from a balloon at intervals:

(Listen to a reproductive pair singing together until about 0:53, when the reproductive male stops. The male offspring joins in with an off-set long note at 0:55. The reproductive female continues her song throughout.)

The indris don't just sing to advertise their presence in a territory to other groups. They actually have three different songs that they sing. 

In addition to the "advertisement song" focused on in this study, the lemurs also have a more chaotic intergroup encounter song, or "territorial song," for when they meet another group along the border of their territories, Gamba explains. The third song is a bit more peaceful. That one is used when members of the same group lose sight of each other in the dense forest within their territory and need to find each other to regroup.

In this new study, Gamba and his colleagues also found "a very clear difference between the contribution of the male and the female within a reproductive pair" to the chorus. Just as male and female humans often speak and sing at different pitches, so do the indris. But among the lemurs, it's the males whose voices hit higher notes more often than females.

"It might be a shared trait with humans that we never understood was in lemur species," Gamba says of the vocal sex differences.

"The study of communication in other primate species is showing a lot of similarities with what we find in humans," and this is an insight that cannot be gleaned from the bones of ancient human species or cave paintings, he says. "The only thing we can do is go into the forest with non-human primates and try to understand how the traits of their communication is saying something about our evolution."

But Wendy Erb, an anthropologist also studying animal communication at Rutgers University who was not part of the study, cautions that the singing lemurs might not be the best link to our own species. "Given the patchy distribution of singing across major branches of the primate family tree, it seems unlikely that the distantly related indri will provide critical insights into the origins of our own species' evolutionary origins of language and music," she tells the Monitor in an email.

Still, she says,"Gamba and colleagues accumulated a truly impressive data set that included observations of 21 indri groups at four research sites made over a 10-year period, resulting in nearly 500 song bout recordings, which the scientists analyzed in painstaking detail... And this research does offer an important contribution to understanding the evolution of vocal coordination within an important branch of primate lineage – the lemurs."

And the pattern of juveniles mismatching their singing with the adults is particularly intriguing, as it is the opposite of what has been observed in gibbons, Dr. Erb says. 

"The fact that co-singing occurs most often between adults and juveniles (mothers and daughters) in gibbons, suggests that vocal learning may play an important role in the development of singing for this group of primates. For indris, the reverse is true, and the relative rarity of co-singing by non-adult indris may indicate that vocal learning is less important for this species," she says. But, "It is too early to conclude whether vocal learning is definitely present in gibbons and fully lacking in indris, but it does raise interesting questions about the influence of cognition, song complexity, and social structure on the development of vocal communication in primates."

"In addition to humans, singing behavior is only known to occur in four groups of primates: indris, tarsiers, titi monkeys, and gibbons," Erb says. "Although singing may not be common among primates, it is found elsewhere in the animal kingdom – most notably among birds – and thus rhythmic abilities, per se, are not a uniquely human feature."