Play's the thing

A garfish jumping over a turtle. From Charles Holder's "Along the Florida reef" (1892)

“the play’s the thing
Wherein I’ll catch the conscience of the king.”
                                                                                             Hamlet, act II, scene 2  

Hamlet, who speaks the lines above, has a problem. In fact, he has lots of problems (it’s sort of his thing), but one in particular that concerns us: Hamlet suspects that his uncle the king murdered his father, but he isn’t sure. The only evidence he has of the crime is the grisly description his father’s ghost gives him, but Hamlet still has questions (Hamlet asks a lot of questions; it’s one of his problems). Like a good scientist, he takes into account the possibility that his suspicions are false (he briefly considers that the ghost might have been the devil in disguise). Hamlet, as many commentators have noted, is paralyzed by this problem: he does not want to kill the king until he is sure his revenge is just. So he devises a plan. A troupe of actors has been engaged to perform at the palace. Hamlet convinces them to stage a play about a duke who is killed by his nephew, who then seduces the duke’s widow. By observing his uncle’s reaction to this not-very-subtle accusation, Hamlet hopes to determine his guilt definitively. The play ploy works perfectly – the king runs off halfway through – and Hamlet’s resolve is strengthened, at least for a while.

I sometimes think of this episode when considering how comparative psychologists work (stay with me). One of our problems is similar to Hamlet’s: when we see an animal perform a particular behavior, we might think we know what it is doing and why, but we don’t have direct access to its motivations (any more than Hamlet does to his uncle’s guilt) so we can rarely be sure. This is why we devise experiments, which are like Hamlet’s play: we expose the animals to situations in which their reactions will, we hope, tell us something about what is going on inside their heads.

Hamlet, however, is not a very rigorous scientist and suffers from confirmation bias. He doesn’t pause to consider all the other, perfectly innocent, reasons that his uncle might have fled the play: maybe he was feeling cold (Danish castles being drafty) or ill; maybe he was bored; maybe he thought that a play about a murder was insensitive so soon after the old king’s death. The rub, as Hamlet might say, is that we can never be sure.

Identifying an animal’s motivation for behaving is a problem all up and down the study of comparative cognition, but nowhere more so than in the field of animal play (as in, “do animals play games?”, not “do animals mount productions of their favourite fables from Aesop?”). There are five criteria that are generally accepted for identifying when an animal is playing: the behavior has to be non-functional, spontaneous or voluntary, different from similar (functional) actions, repeated (but not in an “I’m-losing-my-mind” stereotypical way), and performed when the animal is not stressed [1].

None of these criteria is sufficient on its own, of course, and there are plenty of problems hiding behind the bedchamber curtains when attempting to apply them to a specific action. The first criterion, for example, requires that play behaviors are not functional in their context, but there are lots of non-functional behaviors: If I raise a forkful of food towards my mouth but the food falls off before I can eat it, is that play, or simply incompetence? When monkeys play-fight, is it really simply because they enjoy it, or is it to improve their future position in the group’s hierarchy (which is very functional; [2])?

Hamlet’s problem, however, is what I want to focus on here. Play behaviors, by the second criterion, have to be “spontaneous, pleasurable, rewarding, or voluntary” [3] or “done for [their] own sake” [4]. In other words, we need to identify the animal’s motivation if we are to definitively label some action as playful. But, like Claudius’ guilt*, the animal’s motivation is not directly measurable. Or is it? Can we figure out, from watching the animal behave, what its motivation for a particular action is? This is a controversial topic on which, if I may pluck one more Hamlet quote from its context, “there has been much throwing about of brains” (II.2). The short answer is, we don’t know.

Let’s look at some fish examples. Play in fish has been recognized for quite a while, though there is some debate. A well-known review of animal play behaviors specifically noted that fish do not play [5]. Part of the problem is, as even Gordon Burghardt has acknowledged, that it is nearly impossible to tell when or whether a fish experiences something as enjoyable [4]. Karl Groos, who wrote a book on play in animals in 1895, noted fish’s “exuberance of spirits” [6] and several authors have written of their curiosity [4]. Again, note the problem. Are fish ‘curious’ about a novel object because it’s fun, or are they checking whether this new thing is a predator or food? How would we ever disambiguate those two things?

One of the most famous examples of fish playing is leaping over floating sticks and other small objects. This behavior was described as early as the 1890’s by Charles Holder:

          “Once while lying quietly on the wall of an inclosed aquarium on the Florida reef, I saw a number of
           garfishes... leaping over the back of a small hawksbill turtle which was floating on the surface of the
           enclosure, fast asleep and innocent of the purpose to which it was being put. The animal's back was
           probably eight inches across, and the fishes cleared it several times with ease" [quoted in 4].

The picture at the top of this post, from Holder’s 1892 book, shows this behavior. CM Breder, who also did some of the earliest studies of fish schooling, threw some sticks onto the surface of the water in his experimental tanks and watched needlefish jump over them repeatedly. Well-aware of the problem we are focusing on, he reported that:

         “First the fish will swim up slowly to the stick so as to be nearly at right angles to it... If [the stick]
          is of the proper buoyancy and sinks ever so little under the weight of the beak, a violent tail action
          follows and the fish clears the water, but in such a manner that usually part of the body rubs
          against the stick in passing... It is thought that the function of this well-marked habit is that of
          scratching to remove ectoparasites... Second leaps were most often noted when this did not
          succeed [in scraping the skin]” [quoted in 5].

This brings up a key point. Researchers and enthusiasts interested in play behavior are perfectly well-aware of their definitional problems. We don’t have access to the motivation of the animal; we can’t do experiments on play behavior, because the animals have to perform the behavior ‘spontaneously’ for it to count (and, obviously, it won’t count as play if we reward them for it). Even somehow showing that the animal enjoys the behavior is not enough on its own. As no less an authority than Frank Beach put it: “not all pleasurable activities are playful; but all play is assumed to be pleasurable” [7]. What we don’t have is a good way to overcome these problems, which often leads advocates of animal play to resort to anecdotal evidence and persistence.

Let me leave you with a more recent example, of what is referred to as ‘object play’ in a cichlid [8]. Three cichlids in an aquarium were given a bottom-weighted thermometer which floated near the center of their tank. Over the course of several days, each fish’s interactions with the thermometer were observed and recorded. The fish frequently batted at the top of the thermometer, setting it swinging back and forth, and in some cases they moved it to different parts of the tank or banged it against the glass. All three fish interacted with the thermometer. So, is this play? The thermometer has no functional role (from the perspective of the fish), and the fish were not rewarded in any way for pushing it around. The fish did not appear stressed and they continued to push the thermometer for several days. But was it fun?

Despite the lack of a clear solution to the problems of identifying play, I think that studies like this can’t help but improve our understanding of the range of animal behavior. As the authors of the last study note, “labeling a behavior as play does not explain it... does not end scientific inquiry. The categorization of a behavior with a... label helps us primarily by focusing attention on attributes, causal mechanisms, and adaptive functions that might otherwise have been missed” [8]. So, maybe this is play, maybe not. Our research on this is, of necessity, largely non-functional. As Einstein said, “If we knew what it was we were doing, it would not be called research”. In other words, we’re just playing.
 
 
* That’s right, Hamlet’s murderous uncle is called Claudius, same as the guy that stabbed Caesar. It’s always bothered me
   that he fails to pick up on that hint. Then again, the guy that eventually kills Hamlet himself is called Laertes, same as the
   father of Odysseus. Not someone you want to go up against in a swordfight. This is why history and mythology are
   important, kids.

1. Burghardt GM (2011). Defining and recognizing play. In AD Pellegrini & P Nathan (eds.) Oxford Handbook of the Development of Play (Oxford: Oxford University Press), pp. 9-18.
2. Reinhart CJ, Pellis VC, Thierry B, Gauthier C-A, VanderLaan DP, Vasey PL, Pellis SM (2010). Targets and tactics of play fighting: competitive versus cooperative styles of play in Japanese and Tonkean macaques. International Journal of Comparative Psychology, 23:166-200.
3. Graham KL, Burghardt GM (2010). Current perspectives on the biological study of play: signs of progress. The Quarterly Review of Biology, 85:393-418.
4. Burghardt GM (2005). The genesis of animal play: testing the limits. (MIT Press).
5. Bekoff M, Byers JA (1981). A critical reanalysis of the ontogeny and phylogeny of mammalian social and locomotor play: An ethological hornet's nest. In K Immelmann, GW Barlow, L Petrinovich & M Main (eds.) Behavioral development: the Bielefeld interdisciplinary project (Cambridge: Cambridge University Press), pp. 296-337.
6. Groos K (1895). The play of animals (New York:Appleton & Co) [available online, for your amusement and edification, here].
7. Beach FA (1945). Current concepts of play in animals. The American Naturalist, 79:523-541.
8. Burghardt GM, Dinets V, Murphy JB (2015). Highly repetitive object play in a cichlid fish (Tropheus duboisi). Ethology, 121:38-44.