When picturing animals at play, you probably think of frolicking otters or wrestling tiger cubs--not arachnids aligning their copulatory organs. But University of Pittsburgh researcher Jonathan Pruitt believes that pretend sex between Anelosimus studiosus spiders is a form of play. And, like those wrestling cubs or human toddlers making block towers, the frisky young spiders are gaining skills that will help them in their adult lives. If they devote too much time to play, though, male spiders may never get to experience the real thing.
A. studiosus lives and builds its webs throughout North and South America. The males reach maturity first and leave their homes in search of females. Upon finding a juvenile female spider sitting in her web, a male moves in. While he waits for his love interest to reach sexual maturity, the claim-staking spider attempts to fight off any other males that come by.
But that's not the only activity that fills his time. The male and female engage in courtship and mock copulation--or, as Pruitt puts it, "non-conceptive sexual behavior." Though the female's genital tract is, physically, not open for business, she assumes a "receptive posture" and allows the male to place his parts next to hers.
Lest you suspect that the males are merely a little dim, and keep trying to mate despite the females' physical unavailability, Pruitt explains that mock copulation has clear differences from the real thing. For a start, the spiders are less aggressive with each other than during real sex. Additionally, mock copulation is much less likely to end with the male being eaten. In a real sexual encounter, the male has nearly a 1-in-4 chance of being cannibalized by the female before the deed is done. But males survive almost 99% of dry runs without becoming a meal.
According to Pruitt, this behavior meets criteria for animal play: it takes place in non-stressful situations; it happens frequently and voluntarily; it mimics a functional behavior but doesn't accomplish the same function. In this case, the function that's not being achieved is actual intercourse. But there are other benefits for the mock-mating spiders. Once they mature, pairs in which at least one individual is "experienced" get the job done faster than inexperienced pairs. This presumably helps the male's chances of not being eaten. Experienced males are also less likely to be rejected--or chased out of the web--by females. And experienced females, after they mate for real, lay sturdier eggs.
Pruitt and his colleagues wanted to know which spiders were most likely to engage in pretend copulation, and what the tradeoffs were for those spiders.
The researchers captured baby spiders and grew them to maturity in the lab. By pairing the spiders up and observing how much space they gave each other, the researchers could score each spider's "personality" as docile or aggressive. To study mock copulation, the researchers dropped male spiders onto the edges of female webs and watched each pair for a total of eight hours, counting how many pseudo-sexual encounters occurred. Finally, they dropped new (inexperienced) male spiders onto some of those webs and watched the ensuing face-offs between males.
They found that a spider's propensity for fake mating depended on several factors. Docile spiders were more likely to engage in mock mating when their female partners were large. That's not what one might expect from a species prone to cannibalism, but apparently the males are enticed by large females' greater egg-laying potential.
Among aggressive male spiders, on the other hand, female size didn't matter. Their likelihood of mock copulation only depended on whether their bodies were in good condition.
Aggressive males were also more likely to win competitions with other males, forcing intruders to retreat from their webs. But male spiders that had engaged in a lot of pretend sex, apparently worn out, were less likely to win these duels.
Thus, as Pruitt puts it, "males that engage in the behavior excessively risk exhausting themselves and being supplanted by cohabitating interlopers." (Words to live by.) Though females may mate with multiple males, the male that gets to her first will father most of her offspring. So getting kicked out of one's web by an intruder, even temporarily, can have a high cost.
Is mock copulation in spiders a form of play, or of practice? For animals, they may not be substantially different things. A definition of human play would have to include fun. But whether we're looking at a dolphin or an invertebrate, we can't truly know whether an animal is enjoying itself. Whatever the spider is doing, it's clear that pretend sexual encounters can increase its reproductive success and evolutionary fitness. Unless the male spends too much energy entertaining itself, of course, in which case it may never get to demonstrate its prowess.
Pruitt, J., Burghardt, G., & Riechert, S. (2011). Non-Conceptive Sexual Behavior in Spiders: A Form of Play Associated with Body Condition, Personality Type, and Male Intrasexual Selection Ethology DOI: 10.1111/j.1439-0310.2011.01980.x