Playing Dead: When are Animals Practicing Deception?

I was playing with a spider this morning when this thought occurred to me.

First, here's the game the spider and I were playing: I was sweeping my bedroom, and this spider had been hiding underneath the bed. I discovered him when he tumbled out of his hiding place along with a collection of dust bunnies and popcorn kernels. He nonchalantly skittered off, taking a path that put him in the path of my next sweep. Once again, he was translated across the floor. Taking a moment as if to orient himself, he resumed his path, albeit in a different direction. (Do spiders have a sense of direction? I wondered. Certainly bees do, what with 'the flowers over there' and all that, but ants seem to be largely following each other's scent trails, and as often as not are moving in the wrong direction.) What caught my attention, and provoke my curiosity, was when the spider, after my third playful bat, rolled onto his back and played dead.

Playing possum, we call it. We teach our dogs to do it. Spiders and certain insects do it all the time. But I wondered exactly why the spider was doing it.

Let me be clear as far as my stance on insect intelligence. I can sympathize with people who believe their pets are supremely intelligent creatures: I tend to attribute so-called evidence of this intelligence to coincidence, conditioning, and wishful thinking, but I'll not get into this argument unless I'm feeling combative. But I am confident that the insect mind is so compact, so miniscule, that it simply hasn't got room for critical thinking, advanced logic, and reasoning based on calculating the emotions of others. Not when so many people seem to be lacking in these same skills. So when I see a spider 'play dead', I realize there's nothing in his head that even resembles an internal dialogue, just knee-jerk hard-wired responses. But I still enjoy speculation on the evolutionary justification for these responses, which amounts to a "motivation" or even "intention" of a different sort. Spiders may not have intentions, but spiderdom certainly intends to stick around. If it didn't, it wouldn't be here.

So how does playing hockey puck have to do with survival? (I'm not admitting to batting the supine spider across the floor like a skittle, but let's pretend I had.) My first thought was that he perceived himself as under attack, and his response was intended to convince his would-be predator that he was merely an empty vessel.

But I quickly realized that this was excessively anthropic reasoning on my part. Death might discourage suitors or (sometimes) debt collectors, but it is seldom an effective deterrent to birds or reptiles who are just looking for a few quick calories. Playing dead with a bird is about as effective as playing left-handed with the IRS.

So what is the spider playing at? I have two theories. The first is that he's not playing dead, he's playing gone. Spiders are dirt colored, and spend most of their time walking on other things that are dirt-colored. In many situations, his heels-up attitude would have been nearly as effective as a Romulan cloaking device, especially if I hadn't already spotted him. (And any predator that's unimpressed by card tricks is unlikely to worry to much about a disappearing spider.) There are millions of species, who have adopts being dirt-colored, or grass-colored, or bark-colored, or ocean floor-colored, or excrement-colored as a survival strategy, and most of them have "learned" the complementary art of standing still.

The second possibility is that the spider never gave much thought to me as a potential predator (again, this is selection-pressure thought, not neural thought.) It's possible that spiders got together and decided that, if you're being jerked around from one place to another, whether by wind or a duck or a broom or a flash flood, the best strategy is to hit pause until things calm down a bit. The terminal speed of an insect or spider is so low that they can survive being thrown off twenty-story buildings, or the wings of airplanes, or being flush or sprayed with a hose if they'll just hold tight for a minute. Pull in your legs if you want to keep 'em. It may be that, as important as I consider myself, that spider never even noticed me, not in any sense of the world.

We often talk of the role that deception plays in the animal kingdom. Certainly the moth with owl-like eyespots or the non-poisonous snake with the knock off coral snake paint job is guilty of deception. Ditto if your carapace is shaped like a thorn and you live on a rose bush. But we may overestimate the amount of pure dishonesty if we always assume things are being done for the benefit of an interested observer.

It may be my friend the spider wanted to keep all his legs.