Have you heard this sound in your backyard?

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Maybe you looked up to see a squirrel, chattering away while flicking its tail.

Both the vocalization and the tail flick are alarm signals produced by gray squirrels. It turns out they have a number of vocal and tail signals that have different meanings depending on how they are used.

Thaddeus McRae and Steven Green of the University of Miami looked at whether these different alarm signals were used by squirrels, either individually or in combination, in response to different kinds of threats.

Kuks, Quaas, Moans, Twitches, and Flags

Gray squirrels have three different vocal alarms, which they produce when they spot a potential predator nearby.

The kuk (heard in the example above) is short, sharp, broad-frequency sound. "Imagine a dog barking and then speed it up and shorten it down to squirrel-size," says McRae.

The quaa is essentially a longer version of the kuk, but it can be varying lengths. Both kuks and quaas can be heard in the example below.

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The moan, in contrast to kuks and quaas, is tonal, almost like a whistle.

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In addition to these vocal alarms, squirrels have two types of tail signals. A twitch looks like a wave running through the tail. It's a controlled movement in which the path of the tail tip usually forms a simple arc. A flag is a more conspicuous whipping motion. During a flag (see video below), the squirrel's tail tip can move in arcs, figure eights, circles, and various squiggles.

Sound the Alarm

McRae and Green tested whether these different vocal and visual alarms were associated with particular types of predators. They studied a wild population of gray squirrels on the University of Miami campus. These squirrels have two main types of predators: aerial predators, such as hawks, and terrestrial predators, particularly domestic cats.

The researchers exposed the squirrels to five kinds of potentially threatening stimuli. They simulated a hawk approach by throwing a styrofoam glider painted to look like a hawk in the air. They simulated a cat attack with a remote-controlled model cat on wheels, driven toward the squirrel. To see if the manner of approach (terrestrial versus aerial) or physical resemblance to a predator affected the squirrels' alarms, the researchers also presented the squirrels with an object that didn't resemble any predators at all — a red ball — and either rolled it towards the squirrels or threw it overhead like the model hawk.

Thaddeus McRae, <www.thaddeusmcrae.com>

Overall, McRae and Green found the squirrels have an alarm system with different degrees of specificity. Some, but not all, of the alarm signals were associated with predator type, and combinations of tail signals and vocalizations were more strongly associated with threats than either type of signal alone.

Of the three vocalizations and two tail movements, only tail flags and moans were associated strongly with specific predators. Moans by themselves were specific to the aerially approaching model hawk. Tail flags showed a moderate association with the terrestrially approaching model cat.

Considered by themselves, kuks served as a generic alarm signal. "Whether or not they use kuks doesn't really tell you much about what's going on other than something is upsetting the squirrel," says McRae.

Squirrels made quaas more often in response to terrestrial threats, but sometimes used them when an aerial threat approached, as well.

When McRae and Green looked at the two tail signals by themselves, the twitches were used in lots of different circumstances, sometimes even when there was no predator present.

Considering the vocal and tail alarms together drastically increased one's ability to predict what was eliciting the calls. If terrestrial and aerial attacks are equally common, and a squirrel randomly guesses which type of threat is causing the alarm, it would be wrong about half the time. Looking at whether or not tail flags were used reduces that error rate by about 17%, while looking at whether moans are involved in the signal reduces the error rate by about 20%.

"But paying attention to whether or not they used moans and whether or not they used tail flags reduces the error of their guesses by about 52%," says McRae. "So looking for tail flags while listening for moans reduces your error rate two and a half to three times more than paying attention to only one or the other. The moral is, it's important to both look and listen if we want to know the whole story."

Know Your Audience

The mixed specificity of these signals allows squirrels to adjust the specificity of their alarms and also their own risk of being detected by predators.

Using both auditory and visual alarms together might reinforce the signal, making the alarms more noticeable.

But who are these alarm signals meant for? One possibility is that they function to let other nearby squirrels know a predator is lurking. However, it's also possible that the alarms are meant to let the predator itself know that the squirrel has spotted it.

Broadband sounds like kuks and quaas are easy to localize. These sounds, and conspicuous visual displays like tail flags, advertise the signaler's location. If an ambush predator like a cat knows its potential prey has spotted it, it might give up and look elsewhere for prey it can take by surprise. One study showed leopards stalking monkeys in West Africa left the area more rapidly if the monkeys gave leopard-specific alarm calls. Domestic cats might also be deterred if they know they've been spotted by a squirrel.

Thaddeus McRae, <www.thaddeusmcrae.com>

The narrow-frequency moans are more difficult to localize. Given how specific the moans are to aerial threats, this might be a way for the squirrel to give an alarm call without advertising its location. Hawks can easily take squirrels off the ground or off the trunks and branches of trees, so advertising its location would not be good in the case of aerial predators.

Alerting the predator that the squirrel sees it may be the main function, but that doesn't preclude other squirrels from hearing or seeing the signal and also responding. McRae says he is coming to the conclusion that these alarm calls are used both by other squirrels and to let predators know they've been seen.

Referential or Urgency-Based

McRae has shown that squirrels respond to other squirrels' alarm calls by becoming more vigilant and retreating up trees. However, he doesn't yet know if squirrels respond in unique ways to the different types of alarm signals.

If squirrels did respond differently to alarms that signaled terrestrial versus aerial predators, it might indicate that their alarm system is functionally referential. Functionally referential signals act as if the call refers to a specific object. The call is elicited by this object, and when other animals hear that call, they respond appropriately — as they would to that specific object. For example, if a squirrel consistently gives a particular call when a cat is present and that call elicits anti-cat behavior in other squirrels, then the call functions as if it refers to the cat. (The classic examples of functionally referential alarm signals are those of vervet monkeys, who have specific calls for three different types of predator that each elicit a different and appropriate anti-predator behavior in other monkeys).

Squirrel alarms could also be urgency-based, dependent on factors like how close the predator is and how rapidly it is approaching. McRae thinks it might not be an either/or situation, and the line between functionally referential and urgency-based alarm signals might be fuzzier than it's made out to be.

McRae is currently working on playback experiments to see how squirrels react to alarm signals.

"If they do use different responses, then the signals are functionally referential and these squirrels are basically using these alarms to get predator-specific information and respond accordingly," he says. "But if they don't respond differently to the different alarm signals, that suggests the differences in these alarm calls isn't about being an alarm call but might be directed at the predator."

McRae's research shows there is a lot we still don't know about the behavior of an animal many of us see every day. What other secrets is the humble squirrel hiding?

Reference:

McRae, T. R. and Green, S. M. (2014). Joint tail and vocal alarm signals of gray squirrels (Sciurus carolinensis). Behaviour. doi: 10.1163/1568539X-00003194.

All photos, video, and audio kindly provided by Thaddeus McRae, www.thaddeusmcrae.com.