Non-mammals Like to Play, Too

In April 2013, on board the unmanned spacecraft BION-M, a thick-toed gecko wriggled out of its polyurethane collar. In microgravity, the object floated away, then floated back toward the animal, then away again, approaching another gecko, and then a third. The animals got curious. One pushed the collar with its snout. Another tried inserting its head into it. Yet another pinned the thing down to the floor. As the spacecraft orbited Earth, the geckos started to play.

Russian scientists described this particular instance of reptile play in 2015, after observing the astronaut-geckos with cameras inside the spacecraft. The experiment, designed to study general behavior of reptiles in weightlessness, added to growing evidence that it’s not just kittens and baby chimps that play, but also birds, reptiles, fish and even invertebrates, including spiders and wasps. We have reports of octopuses fooling around with Lego blocks and Komodo dragons waging tug of war with their keepers. In 2015, a study of tooth marks on fossils showed that the bones may have served as a toy for a tyrannosaurid more than 65 million years ago. Play in non-mammalian species offers us novel insights into the activity’s function and evolution. Until recently, however, researchers doubted these diverse species were even capable of the behavior.

For decades, if not centuries, scientists rejected the notion that animals other than mammals actually play, even when faced with observational reports of frolicking fish or apparently fun-loving birds. “People tried to find every possible explanation,” says Gordon Burghardt, a behavioral biologist at the University of Tennessee, Knoxville. “They thought maybe the animals just tried to knock parasites off their bodies, even though there was no evidence they were doing that. Or they’d say that the animals were so stupid they didn’t know the thing they were playing with wasn’t edible, even though you wouldn’t say that about a cat playing with a rubber mouse.”

At the close of the 20th century, as extensive use of video and computers allowed scientists to analyze animal behavior in detail, the consensus began to change. Consider the case of Pigface, a Nile soft-shelled turtle who spent nearly his entire life alone in an enclosure at the National Zoo in Washington, D.C. In the 1980s, when Pigface was already in his 40s, he began biting himself and clawing at his face. “He used to self-mutilate so bad he’d get fungal growth on his skin,” recalls Burghardt. “So the reptile curator thought, ‘Hey, maybe he’s bored?’ No one back then thought that reptiles could get bored.”

In 1991, Burghardt and other researchers gave Pigface two basketballs and a round hoop fashioned from a garden hose, then recorded his behavior. The turtle’s playfulness wasn’t immediately apparent on the video until Burghardt decided to speed up the film. Suddenly, Pigface resembled a frolicking dog: He’d nose, bite, push and shake the toys with his mouth. “That was the first pretty good proof that reptiles could play,” he says. Boredom cured.

Researching non-mammalian play got a boost in 2005, when Burghardt, based on years of research, outlined five criteria defining the activity. That made it easier to qualify if certain behavior was play or something entirely different. According to Burghardt, play is a behavior that is voluntary, repeated several times, doesn’t have an obvious function (so running for fun, yes, but not running away from a predator) and differs in significant ways from regular, functional behavior. It’s also initiated by healthy, largely unstressed animals.

“Play is a kaleidoscope, a mix of different behaviors from lots of different contexts, like predatory behavior, aggressive behavior, sexual behavior, and it’s this mix that allows animals to know that it’s play and not something serious,” says Marc Bekoff, a behavioral ecologist at the University of Colorado Boulder and another researcher whose widely accepted definition of play helped researchers spot this behavior in a broader range of animals.

Play is far from uniform, though, which can make it challenging to recognize. In our mammal-centric ways, we tend to think of play as something that is quite complicated and, as Bekoff says, “cerebral.” But there are many different types of play, some of them simpler than others.

Take ravens, for example. In an experiment published in 2014, researchers from Germany’s Max Planck Institute for Ornithology and Lund University in Sweden observed a group of ravens interacting with a small stuffed mouse and a plastic spider. Sometimes, the birds would manipulate the toys with their beaks or feet — what scientists call object play. Sometimes, if one raven started to play with a toy, another would join — that’s social play. And sometimes, the birds would just hang upside down from a branch, seemingly enjoying themselves.

That’s play at its simplest and most primitive: the running, jumping and romping around that’s defined as locomotion play. No big brain required. A comparison across 15 orders of mammals showed that larger-brained orders contained more playful species. However, within a given order, such as, say, primates, some of the most playful species were those with the tiniest brains.

Regardless of size, play may enhance a brain’s functionality. Experiments done on rats show that play changes the brain, affecting development of the prefrontal cortex, which is responsible for complex thoughts and regulating emotions. In one such experiment published in 2013 by scientists from the University of Lethbridge in Canada, playing enhanced the young rats’ neural plasticity, which helped them to be more flexible in their behavior later in life.

So what if you are a spider and you don’t have a cortex at all? Can you still play? Most likely, yes. “Spiders don’t really have a brain, just a decentralized nervous system with three clusters of neurons,” says Jonathan Pruitt, an evolutionary ecologist who studies spider behavior at the University of California, Santa Barbara. “They can barely see each other, they live in a vibratory world and yet they are doing something that is consistent with what you could define as play.”

In a study published in 2012, Pruitt, Burghardt and Susan Riechert from the University of Tennessee described a peculiar behavior of the Anelosimus studiosus spider. Males and immature females of this species engage in what Pruitt calls “almost-sex,” and they do it over and over again. From a functional perspective, it doesn’t make sense: The females are not yet able to reproduce. The first thought that comes to mind is that the spiders just don’t know they can’t mate successfully, but Pruitt doesn’t believe this to be true. The “almost-sex” differs in quite important ways from the real deal, one of them being that the male doesn’t end up being eaten. Under normal reproductive conditions, there’s a 30 percent chance that a female will eat the male. “But they never kill any of the males during these play interactions,” Pruitt says.

Toning down on aggression is a typical feature of play; it’s even been noted in wasps. Back in 2006, Italian scientists studying young paper wasps noticed that when the insects aggregate in clusters to keep each other warm and survive the winter, they engage in something very much resembling play-fighting in mammals. They beat the antennae of other wasps, lick them and bite them, behaviors that don’t serve any obvious function.

“You don’t need a big brain to play,” Burghardt says. “How it is organized is probably more important. Honeybees have tiny brains and yet they are capable of pretty advanced communication and learning.” It all goes back to how play evolved in the first place.

In the late 1990s, aside from documented incidents among birds, non-mammalian play was still considered a weird idea. Then Jennifer Mather, a psychologist focused on cephalopod behavior at the University of Lethbridge, and her colleague, Roland Anderson of the Seattle Aquarium, gave a few bored octopuses old pill bottles just to see what would happen. And the animals played. They jetted water at the bottles, pushing the “toy” away, waited for it to float back on the aquarium intake’s current and pushed it away again, over and over, seemingly enjoying themselves. This discovery of play in octopuses was fundamental for our understanding of the activity. It suggested that play was not the sole domain of mammals and birds, but that it evolved multiple times throughout the animal kingdom. 

As for why play evolved at all, there is no simple answer. Burghardt believes it may have been, initially, a side effect: If an animal had some excess resources, enough food and time and safety, it might have gotten bored and started to play. Mather thinks this is also the case with octopuses. “It’s an outflow of their curiosity, cognitive ability and their wish to explore the environment — and probably boredom,” she says. The surplus resource theory, as Burghardt calls it, also helps explain why geckos on board the spacecraft started to play while their cousins on Earth — the control group — didn’t. Reptiles depend on external sources of heat, and have a metabolic rate much slower than that of birds or mammals. It’s harder and more costly for them to engage in vigorous activities in normal circumstances. But in space, near-weightlessness made it less energetically costly to play, and so they did.

Burghardt and other researchers also argue that when play first evolved, it didn’t necessarily have any benefits for the animals. It was simply just there. Only later on in the evolutionary process would play — at least in some cases — get added functional value. Sometimes, the benefits would be simple and immediate: exercising muscles, or exploring the environment. Other times, the benefits would be delayed until adulthood. Among the best examples of such a scenario is the almost-sex of spiders: Both females and males who practice this courtship are later more successful in real reproductive behaviors. “They seem to be gaining experience,” Pruitt explains.

All these benefits aside, one question remains unanswered: Are spiders and wasps and geckos actually having fun? In a 2014 paper, Burghardt and his colleagues from the University of Tennessee and the Smithsonian National Zoological Park described how three cichlid fish played with a thermometer in their tank, bouncing the “toy” repeatedly. The animals were clearly playing, but how much (or even if) they were enjoying themselves was impossible to tell. On the other hand, Bekoff and others who have observed ravens rolling down mounds of snow, sometimes doing so on their backs with sticks held in their feet, had a much clearer feeling that fun was involved.

When we observe mammals, telling whether the animals are enjoying themselves appears fairly obvious — we check their body language and facial expressions and compare them to our own — but such an answer is mostly intuitive. Trying to understand the emotions of fish or invertebrates may force researchers to look deeper into what makes play really fun.

Experiments done in rats hint that specific chemical messengers in the brain, such as dopamine and endocannabinoids, may have a role in the pleasure of play. The endocannabinoid system, which is involved in processing sensations such as pain and regulating mood, was once thought to exist only in mammals. But it does occur in fish, birds, amphibians and possibly even in sea urchins. As for dopamine, long known to be a gatekeeper for the brain’s pleasure center, “it’s present in spiders, and we know it has large influence on behavior,” says Pruitt, yet he admits that we still have zero idea whether it could make play fun for spiders.

While the question of spider fun remains unanswered, understanding that play is not limited to mammals changes our perspective on the activity. “One thing we might learn is that play is a very basic behavior and a very needed one in the repertoire of very diverse species,” Bekoff says. “Ant play may be different from dog play, but it may be important for the ants.” And if even octopuses and spiders need play, if it’s indeed such a basic behavior, maybe we should let our own children engage in it more, rather than rushing them from one extracurricular activity to another.

Non-mammalian play may also change our perspective on how much we differ from other species. “I think we have to get rid of some of our anthropocentrism,” Mather says. “The history of science is littered with, ‘Gee, we humans are special.’ And we are not special. You have to realize this when you see octopuses play.”

Marta Zaraska is the author of Meathooked: The History and Science of Our 2.5-Million-Year Obsession With Meat.

[This article originally appeared in print as "The Play's the Thing."]