The Best of Enemies

Predator and prey species shape each other. As Robinson Jeffers put it: “What but the wolf’s tooth whittled so fine/ The fleet limbs of the antelope?” (Actually, if it was the pronghorn antelope he had in mind, it appears that the tooth in question belonged to a long-extinct North American cheetah, but that’s another story.)
For about a quarter-century, scientists at UC-Davis — Richard Coss, Donald Owings, Naomie Poran, David Hennessy, Matthew Rowe, and others — have been studying another predator-prey dyad. The hunter is the northern Pacific rattlesnake; the hunted, the California ground squirrel. The researchers have learned some remarkable things about the coevolution of these adversaries, and of at least one of their neighbors.
Rattlers and ground squirrels have coexisted in what is now California for quite a while; fossil forms ancestral or closely related to the living species have been found in 10- to-12-million-year-old deposits from the Miocene era. There’s a big overlap in their present ranges, although the squirrels have colonized some areas — islands in the Sacramento-San Joaquin Delta, parts of the Central Valley and the Tahoe Sierra — that the snakes haven’t reached.
Much of what the rattlesnake brings to the table — the poison glands and hypodermic fangs, the chemosensory receptors, the heat-sensing pits — is not squirrel-specific. Herpetologist Harry Greene says the viper toolkit originated in Eurasian grasslands 30 million years ago, but Pacific rattlesnakes in California have also evolved ways of reading squirrel behavior. When it enters a squirrel colony, a rattler looks for nesting burrows that contain vulnerable squirrel pups. If an adult squirrel stands its ground when approached, the snake uses that squirrel as the hub of its search pattern, weaving its head and flicking its tongue to lock on to the smell of the pups.
Why go for concealed pups when their parent is in plain sight? Young squirrels are smaller, of course, more manageable mouthfuls for the snake. And for the first three or four weeks of their lives, they’re susceptible to the snake’s venom. But adults are immune, and act like it. They’ll pounce at a rattler, even engage in what the researchers call “substrate throwing” — kicking sand in its face, like the archetypal bully at the beach. Their attacks may even result in the snake’s death.
There’s an interesting thing about the venom resistance, though: it seems to require ongoing selective pressure from rattlesnakes. The Davis researchers have worked out the evolutionary relationships of different ground squirrel populations and calibrated the times they diverged, using geologic benchmarks. Northern and southern subspecies, for instance, were separated about 725,000 years ago when the rivers of the Central Valley began to drain into San Francisco Bay. The scientists also compared how the different populations vary in resistance to rattlesnake venom. Squirrels from the Coast Range near Sunol, with a long history of association with rattlers, ranked higher than squirrels from Davis whose lineage had spent 9,000 years without rattlesnakes in the neighborhood. Populations that colonized those snake-free islands in the Delta about 60,000 years ago showed even lower resistance levels, comparable to Arctic ground squirrels that split off back in the Miocene. Squirrels from Mount Shasta and the Tahoe region also had little or no resistance.
But behavior doesn’t change as fast as resistance in the absence of rattler predation. When Tahoe or Shasta squirrels are introduced to a snake under laboratory conditions, they behave pretty much the same as the highly immune Sunol squirrels, kicking sand and everything. This evolutionary lag could have unfortunate consequences if rattlers were to expand their range into the territories of less resistant squirrel populations. (Squirrel pups less than a month old also act as if they were immune, suggesting that the anti-snake behavioral repertoire is pretty hard-wired. So is the ability to distinguish rattlers from nonpoisonous gopher snakes, demonstrated by captive-reared pups that have never seen either species.) Sand-kicking and other forms of snake harassment seem to be the ground squirrel’s way of assessing how dangerous a snake is. Not all rattlers are equal in this regard. The Davis scientists established in the lab that big rattlers are more of a threat than small ones, and snakes that have warmed up — rattlers, remember, are solar-powered — more than those that are still cold and torpid. The experimental apparatus included, and this is verbatim from the scholarly journal Animal Behaviour, “a squirrel puppet, heated internally to 37 degrees Celsius and rolled in squirrel droppings,” to induce the snakes to strike. Another set of lab trials, intended to measure the squirrels’ response to visual stimuli, involved a lab rat concealed in a green nylon bag, which did seem to elicit a “Good Lord, Martha, what’s THAT?” reaction from the subjects. But they didn’t mistake the ratbag for a snake.
Anyway, it’s easy enough to determine the size and speed of a snake that’s out in the open. But what if it’s holed up in a burrow? Then the squirrels rely on cues provided by the sound of the rattle. Warmer snakes produce higher-amplitude sounds with a faster rate of vibration. Larger snakes produce higher-amplitude and lower-frequency noises. And the squirrels can tell the difference. When recorded rattles were played back from a concealed speaker near the burrows of free-range squirrels, the squirrels reacted with more caution and alarm to the sounds of big warm snakes than to those of small cold snakes.
There’s some evidence that rattlers have been subject to evolutionary pressure to sound big as early in their lives as possible. As a snake matures, the size-related acoustic characteristics of its rattle increase faster than the distance it can strike. Younger snakes are apparently bluffing, sounding larger than life — and more dangerous.
The squirrels’ ear for snake sounds is not infallible; they can be fooled by a bird that sometimes appropriates their burrows as nest sites. California ground squirrels, like other burrowing rodents, are something of a keystone species, inadvertently providing habitat for a bunch of other creatures. Robert Stebbins says the endangered California tiger salamander depends on squirrel excavations for shelter. So does the small, semi-diurnal burrowing owl, which, as it doesn’t usually dig its own accommodations, might better be called the borrowing owl.
The burrowing owl has evolved an uncanny ability to vocally imitate a rattlesnake’s rattle: good enough to deceive ground squirrels, which reacted to recorded owl calls as they would to the rattle of a large warm snake. They were unfazed by other burrowing owl vocalizations, including the bird’s standard scream-chatter alarm call.
The rattle imitation is one of the few examples of acoustic Batesian mimicry (pretending to be venomous or distasteful, like nonvenomous milksnakes masquerading as lethal coral snakes) known in nature. It may serve as a general keep-away warning, not just to squirrels, but to mammalian predators like coyotes and badgers, and even to big herbivores who might be tempted to have a good wallow on top of the owl’s domicile. Observers in Chile, where there are no rattlesnakes, report that the local burrowing owls don’t make the rattle-call.
Predator-prey dynamics can be intricate: rattlesnakes using squirrel behavior to fine-tune their search for prey, squirrels assessing from acoustic cues how far they can push an unseen snake. Each is part of the environment to which the other has had to adapt. But the relationship between reptile and rodent has also created an opportunity for a third party, the burrowing owl, to further its own agenda. Either the cost of mistaking an owl for a rattler is small enough or the mimicry evolved recently enough that the squirrel’s powers of discrimination, impressive as they are, haven’t quite caught up.

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