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DOWN among the walnut trees something stirs. It鈥檚 the breeding season for the
California ground squirrel, and the orchard is dotted with burrows. Out of a
hole comes a careful nose, followed nervously by the rest of the squirrel. It鈥檚
an adult, and female. With a litter of pups in the burrow, she鈥檚 tense and
jumpy. She stands upright, looks around鈥攁nd spots the mottled coils of a
rattlesnake waiting just outside the burrow. Alert now, the squirrel stretches
up to her full height and waves her tail from side to side like a flag.
Suddenly, she dashes towards the snake and kicks sand in its face. Heroic?
Suicidal? Or is there method in her madness?

With its big fangs and powerful venom, a rattler is not something a squirrel
ought to mess with. But what looks like a mad bout of snake baiting is not as
crazy as it seems. It is part of a cool and calculated exercise in risk
assessment. When a rattler is riled it does what it鈥檚 most famous for鈥攊t
shakes its rattle. And that is exactly what the squirrel wants. Although the
rattle is intended as a simple warning that the snake is poisonous, it
inadvertently gives away information a squirrel can use in deciding what to do
about the snake.

And squirrels need all the clues they can get. For a northern Pacific
rattlesnake, a colony of California ground squirrels is a bit like a food
factory. During the breeding season, succulent pups roll off the production line
in handy, portion-sized packages. 鈥淒uring pup season, lots of snakes converge on
a colony. They find a place to coil up and wait for unsuspecting pups to pass
by,鈥� says Ron Swaisgood, a biologist at San Diego Zoo.

While pups are the main prey of northern Pacific rattlesnakes, adult
squirrels are another matter. They are partially immune to the rattler鈥檚 venom,
and will take on a snake in defence of their young. But messing with snakes is
still a dangerous business. 鈥淎 bite can put a squirrel out of commission for a
few days and make it vulnerable to other predators,鈥� says Swaisgood. So before
it goes in fighting, a squirrel weighs up the risks and benefits and then
chooses tactics that are least likely to result in injury.

For the past two decades, researchers led by Don Owings of the University of
California at Davis and Matthew Rowe of the Appalachian State University in
North Carolina have been watching what happens when squirrel meets snake. After
a series of experiments in which they tethered rattlers outside burrows,
silenced rattles with sticky tape, and provoked snakes with fake squirrels on
the end of a stick, they discovered that ground squirrels have a remarkably
sophisticated way of dealing with their snake problem.

Squirrels have a large repertoire of anti-snake tactics. They fluff up their
fur to make themselves look bigger, then loom towards the snake, repeatedly
lunging and retreating鈥攁nd leaping back if the snake looks likely to
strike. Sometimes, the squirrels stand upright, just out of strike range, and
wave their tails. The 鈥渢ail flag鈥� alerts other squirrels to the threat and
encourages them to join in the snake baiting. 鈥淭hey try to encourage the snake
to move on,鈥� says Swaisgood.

Sometimes this harassment works. With its cover blown, the chances of an
ambush are slim and the snake slinks off. If the snake doesn鈥檛 leave, the
squirrel might decide on an all-out attack, pouncing on the rattler and biting
it. Or it might give up and move its pups to a safer burrow. It all depends on
the snake: is it big and dangerous, or small and wimpish? It depends, too, on
what鈥檚 at stake. Squirrels with pups invest more time and energy on anti-snake
manoeuvres. And a snake right on the doorstep suffers more harassment than one
farther from the burrow.

Squirrel-on-a-stick

To assess the risk a squirrel faces when it takes on a snake, Rowe and Owings
made mock attacks with a fake squirrel鈥攁 piece of fun fur rolled in
squirrel droppings and warmed to rodent body temperature. They waved the
squirrel, on the end of a suitably long stick, at snakes of different sizes.
Larger snakes could strike farther and faster and pack a bigger punch with their
fangs, hanging on longer and injecting more venom.

Size, though, isn鈥檛 everything. A snake becomes more dangerous as its
temperature rises. Snakes depend on heat in their environment to regulate their
body temperature. After a cold night, a snake is sluggish, but a couple of hours
in the sunshine will speed up its metabolism, making it quicker and
deadlier.

To find out how much quicker, Rowe and Owings warmed some snakes under an
infrared lamp and cooled others in a fridge. Then the researchers taunted them
with the squirrel-on-a-stick. A rattler with a body temperature of 35 掳C
struck at twice the speed of a similarly sized snake at 10 掳C, and the
fastest snake鈥攂oth big and warm鈥攃ould strike at ten times the speed
of the slowest. Warm snakes also hit their mark more accurately. 鈥淎 rattlesnake
is not just a rattlesnake from a squirrel鈥檚 point of view,鈥� says Swaisgood. 鈥淚t
needs to know about that particular rattlesnake. If it鈥檚 too bold with a big,
warm snake, it will pay a high price.鈥�

And that poses a problem. If a squirrel can see a snake, it might be able to
judge its size, but snakes often lurk in the undergrowth or in burrows. It鈥檚
even harder to tell how warm a snake is by looking at it. 鈥淎 squirrel can鈥檛 wait
to be bitten to find out how quick it is,鈥� says Swaisgood.

Back in the 1970s, Rowe suggested that the rattlesnake鈥檚 rattle might offer
vital clues. Twenty years later, he finally tested the idea. A snake鈥檚 rattle is
made of a series of loosely connected, horny rings. When the snake shakes its
tail, the dry rings knock together, producing the familiar buzzy sound. His
analysis of the sounds made by snakes of different sizes and body temperatures
revealed a clear correlation between the size and state of the snake and the
sound it makes. These differences are not intended to communicate anything in
particular. They are simply the result of physics and physiology.

Larger snakes have bigger rattles, giving the sound a deeper pitch. And
larger snakes shake their tails with more force, generating a louder rattle.
Warm snakes rattle louder than cool ones. They also generate a faster train of
鈥渃licks鈥�. A snake at 10 掳C produces an average of 62 clicks a second, while
a snake at 35 掳C produces more than 200 clicks a second
(see Diagram). 鈥淲e
can just about pick out the individual clicks in a cold rattle but in a hot
snake they blend together to give a continuous sort of hissing sound,鈥� says
Owings.

The clues are there, but can ground squirrels make anything of them? In the
latest series of experiments, Swaisgood staked out an old walnut orchard in
Alameda County, which is home to a colony of ground squirrels and attracts
plenty of snakes. He hid a loudspeaker in a bush and laid a trail of oats
between the entrance of a burrow and the bush. With the bait in place, Swaisgood
retreated to a hide with his video camera, and waited.

Any squirrel that followed the trail was given a blast of taped rattling as
it neared the bush. Some of the rattles were from large snakes, some small, some
warm and some cool. The squirrels鈥� reactions left no doubt that they could tell
what sort of snake lurked unseen in the bush鈥攁nd adjust their behaviour
accordingly. If the rattle was 鈥渂ig鈥� or 鈥渉ot鈥�, the squirrels were very
wary鈥攎ore so with hot snakes than big snakes. They moved around cautiously
and spent a lot of time on their hind legs looking about and waving their tails.
The oats were not enough to tempt them back towards the bush. With cool or
small-sounding snakes, the squirrels were more confident, and returned to the
area more readily. 鈥淲e had no idea how rich a source of potential feedback the
rattling sound was or the sort of details squirrels could extract from it,鈥� says
Owings.

The squirrels quite clearly make use of rattling sounds to size up the enemy.
In more normal circumstances, when there isn鈥檛 a biologist with his finger on
the 鈥減lay鈥� button, a squirrel has to actively seek out information about the
snake. 鈥淚t needs quite a lot of provocation to get it to rattle, and the
squirrels seem to know that what they are doing is likely to provoke a strike,鈥�
says Swaisgood.

Such sophisticated strategies for assessing risk are usually associated with
encounters between animals of the same species鈥攔ivals for a territory or a
mate, for instance. When rivals are equipped with dangerous weapons, such as big
horns, or sharp teeth or claws, the risk of injury is high, so they usually try
to avoid a fight. Instead, they try to gauge which is most likely to win from
other clues that are related to size or fighting ability.

Toads, for instance, have deeper croaks the bigger they are. 鈥淚f a toad hears
a deeper croak then it gives way. It doesn鈥檛 take things any further,鈥� says
Swaisgood. Red deer stags offer several clues. A dominant male will have an
impressive set of antlers and a loud, deep roar. Lesser males read the signals
and stay away from his harem of hinds鈥攁t least to begin with. As the
rutting season progresses and the stag grows exhausted, his rivals move in. They
know when the time is right, because they continually probe for signs of
weakness, roaring at intervals until the owner of the harem can no longer muster
a good, loud answer. Probing enemies for information is especially useful when
an opponent鈥檚 fighting skills change with time. This is true for rattlesnakes
too, which become more dangerous as the day warms up.

Animals of the same species have plenty of opportunity to evolve methods to
assess risk. But when the two animals are predator and prey, this isn鈥檛 supposed
to happen. It isn鈥檛 in the quarry鈥檚 interests to hang around sizing up the
enemy: when it sees a predator, it usually runs. 鈥淎 big tiger is much the same
as a small tiger if you are a rabbit,鈥� says Swaisgood.

A squirrel鈥檚 relationship with a rattlesnake is nothing like that with its
other predators, such as bobcats or golden eagles. Faced with these, it flees.
But squirrels and snakes spend many weeks in each other鈥檚 company. Both animals
can inflict nasty injuries on each other. And encounters between squirrels and
rattlers can last for many hours, giving squirrels plenty of opportunity to
assess subtle clues about the dangerousness of the snake. 鈥淭his sets the scene
for the evolution of the same sort of probing behaviour you see in encounters
between two rivals of the same species,鈥� says Owings.

Old enemies

Like animals of the same species, ground squirrels and rattlesnakes have been
living together for a long time: they have been enemies for around 10 million
years. And at some point during their long evolution together, the squirrels
acquired immunity to the snake鈥檚 venom. 鈥淭his freed them from the normal
constraints of prey and allowed them to be more confrontational,鈥� says
Swaisgood.

While the squirrel has been learning to read the snake鈥檚 rattles, what has
the snake been doing? Rattlesnakes have had just as much time to evolve
countermeasures. And according to Owings, there is some evidence to suggest that
rattlesnakes sound bigger than they really are. The segments of the rattle grow
faster than the rest of the body, so a snake starts to sounds big at an earlier
age. This trick might protect the most vulnerable snakes from attack.

So far, though, rattlesnakes have not found a way to avoid leaking vital
information to the squirrels. For them it is better to rattle than to stay
silent. If a snake doesn鈥檛 rattle, a squirrel will think it is small or cold,
and fair game for a fight. Of course, the squirrel could come a cropper if the
snake turns out to be large, but even big, warm snakes don鈥檛 want to risk a bite
from a squirrel. For them, it is better to warn off the squirrel by rattling
loud and fast. Even worse, a silent rattler could be mistaken for a gopher
snake, which squirrels assault with still greater bravado.

So after 10 million years of coexistence, squirrels seem to have gained the
upper hand in sussing out the enemy. 鈥淣atural selection is probably not so
strong on the snake,鈥� says Swaisgood. 鈥淎fter all, a squirrel stands to lose its
offspring, a snake only stands to lose a meal.鈥�