I’d like to continue Predator Appreciation Month with reflections on one of the more intriguing effects that predators can have on their prey: the development of a vocabulary of alarm. (Or should that be “an alarming vocabulary”?)
Vervets aren’t unique. Other primates — including Diana monkeys and Campbell’s monkeys — also distinguish between eagles and leopards. (Diana monkeys are elegant animals, with fur of several colors. Also, like male vervets and Campbell’s monkeys, male Dianas have a scrotum that’s a tasteful shade of blue.)
Some animals make rather subtle distinctions. Gunnison’s prairie dogs have a different sound for each of coyotes, dogs, hawks and humans. More impressive, they describe what a particular dangerous animal looks like: a human in a blue shirt is announced differently from a human in a yellow shirt. Similarly, meerkats — those charismatic mongooses that stand on their hind legs to scan for predators — give calls that announce both the general type of predator (coming from the sky, coming from the ground) and how close it is — in other words, how urgently everyone should react. Black-capped chickadees — small songbirds that live in North America — have calls that say whether a predator is flying or resting, and if it is resting, how dangerous it is. For example, pygmy owls eat lots of songbirds; horned owls don’t. Sure enough, chickadees kick up more of a fuss about perched pygmy owls than they do about perched horned owls.
In and of itself, it’s not surprising that the sounds animals make are not just noise, or a reflection of the state an animal’s in (scared, happy and so on). But the subtlety of the calls — the full amount of meaning they contain — is only now being appreciated. Decoding animal sounds isn’t straightforward; indeed, alarm calls are among the easiest sounds to study, because the animals hearing the alarms tend to respond in ways that are easy for us to understand and describe — for instance, they stop eating and look about, or run away.
But here’s what I particularly like about all this: animals of one species often respond to the alarms of another. In a small way, it’s like those childrens’ stories that have rats talking to toads, or elephants arguing with ostriches.
Diana monkeys, for example, don’t use the same sounds for “eagle!” or “leopard!” as Campbell’s monkeys do. But they respond to recordings of a Campbell’s monkey shouting “eagle!” or “leopard!” just as they would to a shout from one of their own, or a sighting of the predator itself. Yellow-casqued hornbills — forest birds that have problems with eagles but not leopards — react to Diana monkey shouts of “eagle!” but ignore their cries of “leopard!” (Yellow-casqued hornbills remind me of aging rock stars: their head feathers have that kind of wild look.)
Predators sometimes respond too. After all, alarm calls don’t just let other animals know there’s danger in the area. They can also let a predator know that it’s been seen. Ambush predators, like leopards, often give up and go away once an alarm has been sounded.
Paying attention to the cries and hoots of others can be particularly important for animals that have a bad view of the neighborhood, or that spend a lot of time alone and thus don’t get warnings from their own kind. An example: Gunther’s dik-dik, a species of miniature antelope. These creatures live in pairs, in large territories. They have many enemies — leopards, lions, eagles, hyenas, vultures and the like — and spend much of their time hiding in thickets of undergrowth, where they don’t have a good view. So perhaps it’s not surprising that they tune into the alarm calls of go-away birds — which sit high in the tree-tops, announcing passing predators.
All of this makes sense: you’d expect animals to evolve to pay attention to all the information available to them, especially in matters of life and death. The more important question is, how do they come to know what the different calls mean?
The short answer is, we don’t really know yet. However, there are three basic possibilities. One: they are born with the knowledge — it’s innate. Two: they learn by personal experience, or by watching the fates of others. Three: it’s some combination.
Young vervet monkeys, for example, appear to have an innate tendency to shout “eagle!” — but they do it at anything that’s in the air, be it an eagle, a vulture or a falling leaf. They shout “snake!” at long, thin things on the ground — like twigs. As they get older they learn to refine their calls. This seems to be through positive reinforcement — when they make the right call, adults join in and do it too. (It’s tempting to think there may be negative reinforcement as well. One researcher reported seeing a mother run up a tree after her infant gave a “leopard!” alarm. But there was no leopard — only a harmless mongoose — and when the mother caught up with the infant, she gave it a smack.)
Moreover, many animals are quick to make associations between sounds and danger. In areas where wolves have been absent and then reintroduced, female moose that have lost a calf to wolves are much more attentive than other females to the sounds of wolf howls. Perhaps dik-dik fawns see their parents reacting to the cries of the go-away bird, and learn to do it too.
This subject is not merely of academic interest. Many programs in animal conservation depend on reintroducing captive animals to the wild. But if an animal doesn’t know what to be afraid of, it probably won’t last long Out There. Understanding how animals acquire fear of predators — and then teaching them what to be afraid of, and what to listen out for — may be essential if newly freed animals are to survive.
For vervet monkeys responding differently to different alarms, and for young vervets being trigger happy, see Seyfarth, R. M., Cheney, D. L. and Marler, P. 1980. “Monkey responses to three different alarm calls: evidence of predator classification and semantic communication.” Science 210: 801-803; for a more lengthy, and fascinating, discussion of all this, see Hauser, M. D. 1996. “The Evolution of Communication.” MIT Press. (The description of a young vervet being smacked by its mother for making the wrong call is given on page 309.)
For Diana monkeys making different sounds for leopards and eagles, see Zuberbühler, K., Noë, R. and Seyfarth, R. M. 1997. “Diana monkey long-distance calls: Messages for conspecifics and predators.” Animal Behaviour 53: 589-604. For the same phenomenon in Campbell’s monkeys, see Zuberbühler, K. 2001. “Predator-specific alarm calls in Campbell’s monkeys, Cercopithecus campbelli” Behavioral Ecology and Sociobiology 50: 414-422.
For human shirt colors being announced by prairie dogs, see Slobodchikoff, C. N., Paseka, A. and Verdolin, J. L. 2009. “Prairie dog alarm calls encode labels about predator colors.” Animal Cognition 12: 435-439. For meerkats giving information about predator type and the urgency with which listeners should respond, see Manser, M. B., Seyfarth, R. M. and Cheney, D. L. 2002. “Suricate alarm calls signal predator class and urgency.” Trends in Cognitive Science 6: 55-57. For different call types in black-capped chickadees, including assessments of predator danger, see Templeton, C. N., Greene, E. and Davis, K. 2005. “Allometry of alarm calls: black-capped chickadees encode information about predator size.” Science 308: 1934-1937.
For an interesting discussion of the difficulties in interpreting animal noises, see Hauser, M. D. 2000. “A primate dictionary? Decoding the function and meaning of another species’ vocalizations.” Cognitive Science 24: 445-475.
For Diana monkeys understanding the calls of Campbell’s monkeys, see Zuberbühler, K. 2000. “Interspecies semantic communication in two forest primates.” Proceedings of the Royal Society of London B 267: 713-718. For yellow-casqued hornbills tuning into Diana monkey shouts of “eagle!” but not “leopard!” see Rainey, H. J., Zuberbühler, K. and Slater, P. J. 2004. “Hornbills can distinguish between primate alarm calls.” Proceedings of the Royal Society of London B 271: 755-759.
For leopards giving up when they realize they’ve been detected, see Zuberbühler, K., Jenny, D. and Bshary, R. 1999. “The predator deterrence function of primate alarm calls.” Ethology 105: 477-490. For an excellent general overview of what we know about alarm calls, see Zuberbühler, K. 2009. “Survivor Signals: The Biology and Psychology of Animal Alarm Calling.” Advances in the Study of Behavior 40: 277-322.
For Gunther’s dik-dik responding to calls of the go-away bird, see Lea, A. J. et al. 2008. “Heterospecific eavesdropping in a nonsocial species.” Behavioral Ecology 19: 1041-1046. For moose that have lost calves to wolves becoming sensitive to wolf calls, see Berger, J., Swenson, J. E. and Persson, I.-L. 2001. “Recolonizing carnivores and naïve prey: conservation lessons from Pleistocene extinctions.” Science 291: 1036-1039. For a review of animals learning about predators by observing others, see Griffin, A. S. 2004. “Social learning about predators: a review and prospectus.” Learning and Behavior 32: 131-140. For an example of how pre-release predator training can help captive-reared animals to survive in the wild, see Shier, D. M. and Owings, D. H. 2007. “Effects of social learning on predator training and postrelease survival in juvenile black-tailed prairie dogs, Cynomys ludovicianus.” Animal Behaviour 73: 567-577.
Many thanks to Dan Haydon for insights, comments and suggestions.