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Snakes, Squirrels, and Signals: A Tale of Tails

Getting fancy in front of your enemies can be dangerous. Just ask Anderson Silva, the former UFC Middleweight champion who lost his title to upstart Chris Weidman in July. Silva, famous for showboating and taunting his opponents in the ring, let his guard down and Weidman quickly took advantage, ending Silva’s 7-year reign as champion. But many animals regularly perform elaborate displays in the face of danger – displays that would seem to place them at risk – and animal behavior researchers have debated the function of such behaviors for decades.

A California ground squirrel in central California. Photo by Neil Losin.

A California ground squirrel (Otospermophilus beecheyi) in central California. Photo by Neil Losin.

One of the best-known examples of a flashy defensive display is a gazelle behavior called “pronking,” “stotting,” and other indelicate-sounding names. What is pronking? When a gazelle spots a predator like a cheetah, it will leap high into the air with its back arched and all four legs extended downward (here’s a nice video that shows several springbok pronking when they detect a hunting family of cheetahs). Pronking slows a gazelle down and makes it very conspicuous; it certainly isn’t an evasive maneuver per se. Indeed, the word “pronking” even has its roots in an Afrikaans verb that means “to show off.” So why do gazelles pronk? The evidence suggests that pronking may actually send a message to predators: “I’m fast, so don’t bother chasing me.”

Another well-known defensive display is familiar to many residents of the western U.S. The California ground squirrel (Otospermophilus beecheyi) waves its bushy tail from side to side when confronted by a Pacific rattlesnake (Crotalus oreganus) (click here for video). Naturalists first described this behavior in the early 20th century. But while we know a lot about the interactions of squirrels and rattlesnakes (thanks largely to the work of Richard Coss and the late Don Owings, researchers at UC Davis), we still don’t fully understand the functions of this “tail-flagging” display. Why would a squirrel that’s facing down a rattlesnake want to draw undue attention to itself?

San Diego State University researcher Bree Putman. Don't worry, that's not a rattlesnake!

San Diego State University researcher Bree Putman. Don’t worry, that’s not a rattlesnake!

“Upon first glance, what they’re doing just seems maladaptive,” says biologist Bree Putman. “But that’s what’s so fascinating – why do they approach so close? And why don’t the snakes strike them when they’re so close?” Putman and her collaborator Rulon Clark, researchers at San Diego State University, presented some of their latest findings on the tail-flag display at the 2013 Animal Behavior Society meeting in Boulder, Colorado. Putman and Clark were particularly interested in testing two hypotheses:

  • Perception advertisement: The tail-flag is a signal that tells the snake that the squirrel has detected it.
  • Vigilance advertisement: The tail-flag is a signal that tells the snake that the squirrel is alert and ready to flee.

Rattlesnakes are ambush predators, so their hunting strategy depends on them not being detected. If a rattlesnake’s prey sees the snake and prepares to escape, then the snake’s odds of success diminish.

Putman and Clark set out to test these two hypotheses with a simple two-part experiment. In the first part, they trained wild squirrels to visit “bait stations,” where the squirrels could eat seeds provided by the researchers. Each squirrel was exposed to one of three conditions: 1) A live rattlesnake was added near the bait station, but restrained so that it couldn’t actually strike the squirrel; 2) No rattlesnake was added (a “control” condition); and 3) A rattlesnake was added, as in condition (1) above, but it was then removed. In this final condition, squirrels were “primed” – vigilant against a possible rattlesnake attack, but uncertain of the snake’s exact location. During this first part of the experiment, the researchers would observe the squirrels’ tail-flagging behavior in each condition.

A Pacific rattlesnake (Crotalus oreganus) in southern California. Photo by Neil Losin.

A Pacific rattlesnake (Crotalus oreganus) in southern California. Photo by Neil Losin.

Then, in the second part of the experiment, Putman and Clark would simulate a rattlesnake strike. Why not use a real snake strike? First, you can’t tell a rattlesnake when you want it to strike, and the researchers needed to control the strike’s timing. Second, if a snake hits its target, your research subject is in serious danger! And finally, condition (3), described above, requires that no snake is present at the time of the strike. Schrödinger notwithstanding, a snake can’t be present and absent at the same time.

Clearly, some kind of serpent surrogate would be required. Clark came up with a clever idea. There is already a device, he reasoned, that was designed to simulate a snake strike… The old “snake-in-a-can” gag has been scaring the bejeezus out of unsuspecting victims, especially the ophidiophobic among us, for generations. Developed by slapstick innovator Soren Sorensen Adams back in 1915, the snake-in-a-can prank has been a comic staple among children and immature adults ever since (although its popularity was ultimately eclipsed by that of Adams’s magnum opus, the Joy Buzzer, which – after a decade and a half of intense R&D – was unleashed by the S. S. Adams Company in 1932).

If the snake-in-a-can prank is good enough to fool a person – at least temporarily – would it also be good enough to fool a California ground squirrel? “If they’re concerned about a snake strike,” Putman explains, “they should respond to any fast-moving object that’s coming their way.” But Putman and Clark wanted their snake-strike stimulus to be as realistic as possible. They acquired a snake-in-a-can toy and measured the fake snake’s velocity with high-speed video. Amazingly, with no modifications, the snake-in-a-can’s strike velocity was virtually identical to that of a real rattlesnake. The researchers loaded their spring-loaded “snake” into a length of PVC pipe, added a triggering mechanism to launch the strike at their command, and attached a cork to serve as the dummy snake’s “head” (and cushion the blow if a squirrel actually got hit). They were ready for the experiment!

Putman and Clark’s experiment involved more than 60 squirrels, divided evenly among the 3 conditions described above: snake present, snake absent, and snake “primed.” Based on these data, they presented an intriguing set of preliminary findings.

Biologist Bree Putman prepares a spring-loaded "snake" for an experimental trial.

Biologist Bree Putman prepares a spring-loaded “snake” for an experimental trial.

Before the simulated strikes, the squirrels’ behavior provided evidence supporting the perception advertisement hypothesis; squirrels were more likely to tail-flag if a snake was present than if no snake was present. But squirrels in the “snake-primed” group were also more likely to tail-flag – even after the snake was removed from the bait station – than squirrels that were not exposed to snakes at all, suggesting that the perception advertisement hypothesis wasn’t the whole story.

When the spring-loaded snake struck, the squirrels wasted no time; the reaction times of tail-flagging squirrels averaged about 39 milliseconds. That’s really, really fast. To put that number into perspective, consider that an Olympic sprinter takes about 130 milliseconds – three times as long – to react to the starting gun. In fact, modern timing systems actually disqualify runners who begin to push off the starting blocks less than 100 milliseconds after the starting gun; it is widely believed that no human can react in less than 100 milliseconds. (British sprinter Linford Christie, then the defending Olympic champion at 100m, was disqualified from the 100m final in the 1996 Atlanta games based on just such a “false start” after the starting gun, causing considerable controversy.)

What about non-tail-flagging squirrels? They didn’t react as quickly as tail-flagging squirrels, providing support for the vigilance advertisement hypothesis: the data suggest that squirrels that didn’t tail-flag were less vigilant as those that did. The actual difference in reaction time was small – 39 milliseconds versus 51 milliseconds, on average – but even a few milliseconds probably makes a difference when a rattlesnake strikes at close range!

Interestingly, when Putman and Clark compared snake-primed squirrels to those in the other two conditions, the snake-primed squirrels reacted and propelled their bodies out of harm’s way more quickly. Part of the reason may be that snake-primed squirrels often used an acrobatic “dodge” maneuver to escape, while non-primed squirrels – whether a snake was present or not – rarely dodged, preferring instead to “scramble” away on the ground. Based on the high-speed video that Putman and Clark collected, the dodge (a kind of aerial somersault; “I call it the ninja move,” Putman admits) was usually faster than the scramble.

So, in addition to providing support for both the perception advertisement and vigilance advertisement hypotheses, Putman and Clark’s experiment suggests something else, something to which we can all relate: that uncertainty can be unsettling. California ground squirrels may be more vigilant when they suspect a snake is present than when they know a snake is present. “The snake’s effective strike range is pretty small,” says Putman. “So as long as [the squirrels] can see the head of the snake, they can keep their distance. But when they don’t know where the snake is, they get a little bit more freaked out.”

So if you’ve been reading this article about squirrels and thinking that Game of Thrones wasn’t going to make an appearance, you’re wrong. Because George R. R. Martin’s words seem to ring uncannily true for California ground squirrels:

“The unseen enemy is always the most fearsome.” – George R. R. Martin, A Clash of Kings

California ground squirrels and Pacific rattlesnakes have become a “model system” for studying interactions between predators and prey. “It’s really amazing,” Putman says, “because it’s this coevolutionary ‘arms race,’ where squirrels have evolved this arsenal of defenses. It’s not just the ‘dodge.’ They have resistance to venom. They heat their tails in response to rattlesnakes [which, being pitvipers, locate prey using heat-sensitive pits on their faces] but not to other snakes.” Even after decades of research and dozens of research papers about ground squirrels and rattlesnakes, however, there are still plenty to puzzles left for researchers to solve. And this, it turned out, was a recurring theme at the Animal Behavior Society meeting: even in the behavior of the most familiar organisms, mysteries abound.

N.B. Using an actual snake-in-a-can toy as a snake substitute for research might sound a little silly. But by using a commercially available product, rather than developing a custom device, Putman and Clark saved themselves (and their funders) a lot of time and money. Recently, certain politicians have characterized some animal behavior research as “wasteful government spending,” and have taken aim at a handful of NSF-supported research programs because their methods, when taken out of context, can sound rather funny. In fact, there was a special session at this year’s Animal Behavior Society meeting about “Defending Basic Research” against such attacks. Needless to say, I don’t think these attacks on science are well founded. But I will revisit this topic in a future post.

References:

Barbour, M. A. and R. W. Clark. 2012. Ground squirrel tail-flag displays alter both predatory strike and ambush site selection behaviours of rattlesnakes. Proc. R. Soc. B. doi:10.1098/rspb.2012.1112

Putman, B. J. and R. W. Clark. 2013. Testing the function of an antipredator display: ground squirrel tail-flagging toward rattlesnakes. Paper presented at the 2013 Animal Behavior Society meeting in Boulder, CO.

Check out the Clark Lab website and Bree Putman’s research blog to learn more.

Neil Losin is a National Geographic Explorer based in Boulder, Colorado. Neil has a Ph.D. in Biology from UCLA, and is also an award-winning photographer, writer, and filmmaker. This is the first in a short series of blog posts highlighting the fascinating animal behavior research presented at the 2013 Animal Behavior Society meeting in Boulder, Colorado. To learn more about Neil’s other science-media projects, visit www.daysedgeproductions.com.

Comments

  1. Ima Ryma
    August 14, 2013, 6:07 am

    Being a squirrel, I wave my tail.
    Humans grabbed me to check this out.
    Why do I wave it when I hail
    A rattlesnake that comes about?
    Humans think it a silly thing,
    That I would act with a snake so.
    Aren’t I worried the snake will spring,
    Because I’m doing my tail show?
    So the humans bribed me with treats,
    To wander where a “snake’ would be,
    To observe my tail waving feats.
    I played along, but that’s just me.

    There’s nothing much sillier than
    Humans with a snake in the can.