Suomen Kulttuurirahastolle: liite apurahahakemukseen

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Chapter 6. Laughing rats and other playful animals


A silver-coloured ring glimmers faintly, submerged in turquoise water. A torpedo-like shape darts from the depths, stopping just short. A leisurely turn of the body reveals the torpedo as a dolphin, now giving the ring a few delicate nudges with its snout and watching how the surface of the ring starts to quiver. Some more nudges, then an intense push. The ring wobbles and changes shape, but still remains intact – until the dolphin turns around and takes aim. With one exuberant swing of the tail fluke, the dolphin shatters his toy into a myriad air bubbles. The dolphin then dives deeper, takes a U-turn near the bottom of the pool, and blows a new series of bubbles from his blowhole – the dolphin version of nostrils, located on the back of his head. With a quick sweep of his snout, he joins up the fresh bubbles to form a new ring.

Dolphins making toys out of air is far from a common sight. However, it is real: this phenomenon has been observed in a handful of dolphinaria around the world. The dolphins haven’t been trained to do this trick; it’s a pastime they’ve invented by themselves.

Blowing bubbles as such is an ordinary part of being a dolphin. Surprised, vocalizing or squabbling dolphins often releases series of bubbles from their blowholes, the nostrils located on top of their heads. Dolphins in the wild also produce “curtains” of bubbles to help them round up shoals of fish. But some dolphins living in captivity have discovered you can also craft rings of air by joining bubbles.

These rings are only used as playthings, and not for anything useful. Dolphins may join them up to form larger rings, swim through them, or shatter them by swatting them with their tail flukes or flippers. Most of these observations have concerned bottlenose dolphins, the species most commonly kept in captivity. But belugas, their large pale cousins, have also been observed slowly blowing large bubbles and toying with them. Such deliberate preparations for play are quite uncommon in the animal kingdom. These dolphins and belugas are not just playing with air, but constructing toys for themselves.

Giggling in ultrasound

The most widely publicised examples of scientific studies of animal play concern “laughing rats”. Professor Jaak Panksepp, an Estonian-born American psychologist and neuroscientist currently at the Washington State University, has studied a range of problems such as the causes of autism in humans, but he is also a pioneer in the science of animal emotions.

One day in the late 1990s, Panksepp and his student Brian Knutson started to wonder about a strange chirping noise they had recorded while their rats were absorbed in rough-and-tumble play. The sounds were only audible using an ultrasonic microphone, because they were too high-pitched to be audible to the unaided human ear. The upper limit of human hearing is at a frequency of approximately 20 kilohertz. Rats scream their warning signals at 22 kHz. The mysterious chirping noise detected while the rats were playing with abandon was as high-pitched as 55 kHz, which is way out of our hearing range.

Panksepp and Knutson eventually found out they could actually elicit this sound by tickling the rats. Ultrasonic eavesdropping on rats in mutual play revealed that they started chirping already slightly before engaging in actual play. Even solitary rats playing by themselves made some chirping sounds, but these noises were much more evident when the rats played with each other. Their play sessions also appeared to be quite memorable. Many rats were observed suddenly starting to chirp when placed alone in an empty cage where they had previously played with a familiar rat. When placed in identical, equally familiar cages where they had never spent time with a playmate, they remained silent. Panksepp and Knutson concluded that such chirping can express rats’ anticipation of play, as well as the emotions they experience during play.

Can this give us a glimpse into what it’s like to be a rat playing? Is there any way to find out whether this twittering sound is produced as mechanically as if a machine were making it, or whether the rats actually feel something? One of the standard methods used by scientists to find out whether an animal has experienced pleasure is to test whether it attempts to get into the same situation again, even in cases where the situation yields no other benefit such as food. Experiments by other researchers, such as Daniel Calcagnetti and Martin Schechter of Northeastern Ohio University, have shown that playful rats do just this. When juvenile rats are allowed to vote with their feet, they typically try to find their way to the same locations where they have previously played with other young rats. Further clues about rats’ experiences can be gleaned from their brain chemistry. Just before rats start playing, there is a surge in the secretion of dopamine in their brains. In humans, this neurotransmitter plays a role in attention-seeking and pleasure-seeking. During their play, rats then experience an increase in the secretion of endogenous opioids, which in humans would result in us feeling pleasure.

Panksepp dubbed these play vocalisations “laughter”. In his own writing, he usually uses quotation marks. In media coverage, the quotation marks have typically been left out. One can ask whether laughter is the most accurate word to describe the rats’ utterances, because human laughter is a reaction to something that has already happened, such as a joke or a tickle. Rats start chirping when anticipating play, so the sound can also be an invitation to play. But regardless of whether rats are reacting to play or inviting it – or perhaps both – the chirping appears to be a genuine indicator of their emotions. This would make it more similar to a human smile, of the sincere type that involves the corners of the eyes. This ultrasound twittering could therefore be one of the most promising avenues into the private world of rats’ experiences.

How can we recognize real play?

Sounds and gestures indicating playful intentions come in handy for other species than humans. To be able to start a play session in the first place, an animal needs some way to communicate that the following attack is not meant to be a murder attempt. A play-soliciting kitten bounces sideways, with its legs stiff, as if on springs. It then leaps onto a sibling, also as theatrically as possible, with an arched back and pawing at the air. The whole scene seems to be exaggerated and in slow motion at the same time. To emphasize its amicable intentions, the kitten may also cut short its leap short, to land just in front of its playmate instead of flattening him.

Most dog owners are familiar with the “play-bow” gesture. A dog invites another to play by rapidly pressing its front half down to the ground, while leaving its hindquarters standing tall, maximizing the visibility of an enthusiastically wagging tail. Some dogs also sport a smile-like facial expression that is easy for humans to relate to.

Our closest relatives, the chimpanzee and the bonobo, use a “play face” expression whose meaning is equally obvious to us, with their mouths slightly open and drawn to either side at the corners. But when it comes to more exotic facial expressions and body shapes, it becomes harder for us humans to reliably recognise which animal gestures signify playfulness. For instance, we are accustomed to our own pace of life, so we tend to expect play to manifest itself in rapid movements. But dugongs and manatees, also known as sea cows, do everything slowly. Some scientists suspect that the way they sometimes slowly and elegantly circle around each other is a form of social contact resembling apes’ grooming. But another possibility is that this underwater ballet may be the way that dugongs and manatees play chase.

There another reason why behaviour in the animal kingdom can easily looks more serious than it really is. For animals the tiniest hint of danger is enough to dispel a playful mood. In the wild, animals usually become aware of us far earlier than we spot them. In the vast majority of cases, animals will have interrupted any playful antics before a human spectator arrives on the scene. Researching animal behaviour in the wild often requires months of camping out in the vicinity of the subjects, gradually habituating them to the presence of scientists, before the animals relax enough to reveal the full complexity of their lives.

Patience brings rewards. Professor Tim Caro of the University of California is one of the scientists for whom wild natural habitats are his second home. One of his research projects has involved spending thousands of hours observing the play behaviour of wild cheetah cubs in Tanzania. At the age of two months, cheetah cubs look a bit like sturdily built kittens with overgrown legs, except for the light, downy punk-style hair protruding from their heads and backs. Their behaviour resembles that of kittens even more than their appearance. The cubs spend an average of an hour a day just romping about. Their most popular games include leaping at siblings, slapping each other with their paws, and other versions of hunting each other. Sudden sprints and turns are common, as well as the “bounding run” characteristic of young cheetahs: a slow, rocking stiff-legged jogging motion. As the cubs get older, they start finding inanimate objects increasingly interesting, and expand their play to dragging around bones and strips of skin.

There are countless other examples of the ways animals play. Bear cubs roll on the ground and wrestle with each other. Juvenile ground squirrels pounce on each other from a running start, or compete in boxing matches using their forepaws. But how do we know this is play? What if the bear cubs just cannot walk properly yet, or the ground squirrels are really fighting? If an activity looks amusing to a human observer, it’s all too easy to see it as play even when the animal is actually experiencing something else entirely. For this reason, scientists specializing in animal play have striven to develop criteria to distinguish genuine, deliberate play from other incidents.

The most widely used solution model is a set of five criteria developed by Professor Gordon Burghardt of the University of Tennessee, a leading scientific authority on animal play. To qualify as real play, an animal’s activities have to meet all five criteria simultaneously. The first requirement is that the behaviour is not fully functional in its context. For example, the target of an attack may be useless, such as a when a predator attacks a stone. Secondly, the behaviour should be spontaneous, voluntary, or otherwise free from any external reward or compulsion. Thirdly, there must in addition to the mismatch between the behaviour and context (as in the first criterion and the example of the stone-stalking predator), the behaviour should also be incomplete, exaggerated or otherwise different from the “serious” version of the same behaviour. A typical example involves a kitten or puppy engaged in the predatory ambushing of a sibling, with the final killing bite thankfully edited out of this behavioural sequence. The fourth requirement is repetition with modification. The animal performs the activity again, and again, but experiments with various versions instead of faithfully reproducing its previous actions. The last criterion concerns the environment as well as the animal itself. Playing requires a so-called “relaxed field”: the animal should be well-fed, healthy and free from stress factors such as nearby predators. Each of these criteria is vital when it comes to understanding whether an animal’s mind really is in a playful mode, as we will soon see.

Does uselessness equal fun?

A dog is spinning frantically round and round on the floor, trying to catch its tail. To no avail; the tail repeatedly escapes just as quickly. Such behaviour often looks funny to us, and dog owners have posted thousands of videos of it on YouTube. Recently a set of such YouTube videos has been used in a scientific study analysing the behaviour of tail-chasing dogs, by Charlotte Burn and Verity Browning of the Royal Veterinary College in the UK. Their analysis showed that fewer than one fifth of the videos fulfilled the five criteria for animal play. Many of these videos involved puppies instead of adult dogs. The majority of cases were quite different. Almost three-quarters of the dogs in the videos kept spinning like robots, following exactly the same trajectory. This revealed that something far more serious was going on. Owners were often heard laughing on the videos, even when the dogs collided with furniture, but most of the adult dogs were clearly not playing.

Tail-chasing in dogs is in many cases a form of stereotypic behaviour. This involves continuous, painstakingly precise repetitions of a movement that has no obvious purpose. The most common place for most people to see such behaviour are those zoos in which animals are kept in rather small, barren cages. A tiger or leopard may pace back and forth endlessly, tracing exactly the same route, always turning at precisely the same spot. There is a range of causes that can make an animal exhibit stereotypy, such as frustration in an environment lacking anything meaningful to do, or a sense of fear, pain or other physical discomfort. Not all individual animals become stereotypic even under the worst living conditions. Those that do have fallen into a kind of trap made of brain chemistry. When animals fail to adapt to their environment – which may be too stressful, too barren or otherwise badly fail to meet the animal’s basic needs – some of them notice that mechanical repetition of aimless movements makes them feel slightly better. This is because such repetitive movements trigger the release of small quantities of endorphins, the brain’s own “pleasure chemicals”, which provide momentary relief. In the long run, stereotypic behaviour further worsens animals’ welfare, as they become addicted to the momentary relief from anxiety. Addictions erode an animal’s ability to derive pleasure from the ordinary little joys of life, as they do for humans.

Different species resort to different kinds of stereotypic behaviour. Cows tethered so they cannot walk often end up rolling their tongues. In fur farms, the most common stereotypy among minks involves continuously running back and forth: within just a couple of leaps a mink can jump the length of a standard cage, then turn around, take a couple of leaps back, and then start again. Running wheels, often regarded as toys for animals, are not always as beneficial as they might seem. Providing farmed minks with running wheels in an experiment resulted in some minks substituting their stereotypic back-and-forth running with equally stereotypic wheel running. We humans are no strangers to stereotypic behaviour in cases where things go badly enough. One of the most common stereotypies in children is rocking. Such behaviour is especially visible in some autistic children and among children raised in poor-quality orphanages.

The five criteria for play therefore have more than academic value. They can reveal when an animal is not really having fun at all, but instead sending out alarm signals related to mental problems it is suffering from due to an unsuitable environment. The reason why some people mistake stereotypies for play is the uselessness of the behaviour. But there is a tell-tale clue in this context. One of the five criteria for play is absent: modified versions of the activity.

Predatory make-believe

Many cats play with objects not only as kittens, but well into their adult lives. Small objects with quick, erratic movements, such as ping-pong balls or toys on a string made “alive” by their owners, are common favourites. As the toy comes into view, the cat instantly becomes alert and fixates her gaze on it. Crouching down, the stalking cat creeps ever closer to the unsuspecting toy. Once close enough, she briefly adjusts her hind paws into an optimal position, pounces, and catches the “prey” with her front paws.

No matter how absorbed a cat is in preying on a ping-pong ball, most people find watching playful kittens far more entertaining and cute. There is a good reason; often such behaviours of a kitten and an adult cat are really two different things. A kitten bounces around, leaps dramatically on top of a playmate, or grasps for a feather using unnecessarily complicated manoeuvres. With all this experimentation and variation, kittens’ antics are genuine play. As kittens grow up, they tend not to fool around like this so often. Their interactions with toys increasingly look more like serious predation.

Some adult cats retain a penchant for actual play, in the sense that they continue to vary their movements and experiment with the world around them. However, the commonest sequence of action by far – stare-stalk-prepare-dash-catch – is so similar to real predatory behaviour that it would be easy to imagine an unlucky mouse in the place of the toy. The types of toys cats find fascinating are also telling. The best way to get full feline attention is for the toy to be very small, and to scurry across the scene in a series of dashes and halts like a wary rodent, even if it is only being pulled on a string by the cat’s owner.

Some researchers suspect that when we think an adult cat is playing, what is actually going on in her mind is something else entirely: something that fulfils her behavioural needs. Behavioural needs, which will be examined later in this book, are genetically determined, hardwired “programmes” within an animal’s brain. They result in powerful urges for specific activities, crucial for survival and reproduction in the wild. Natural selection has favoured such behaviour. The most ardent and practised hunters are the best at getting themselves and their cubs fed. Throughout millions of years of evolution, behavioural needs have become cemented as an inborn part of animals’ mental experiences. The minds of domestic animals are still very much affected by their wild ancestors’ behavioural needs, almost unchanged. Thwarting these behaviours leads to frustration and poor welfare – even when an animal has spent its whole life in a cage and we think it ought to be “accustomed” to such circumstances.

A cat stalking a ball obviously knows the ball is not a mouse. Otherwise she would try to eat it. But she also knows that stalking and pouncing make her feel good. Some cats enjoy playing with toys even if they have access to the great outdoors, with all its real-life rodents. But access to enticing mouse substitutes is especially important for indoor cats. The absence of little things scurrying about in ways that would trigger their predatory behaviour forces them to seek other ways to get pleasurable experiences.

The search for pleasure in itself is another programme hard-wired into the brain. It originally evolved to ensure that behaviours vital for survival are practised frequently enough. When animals lack the feeling of normality resulting from sufficient pleasurable experiences, some go to great lengths to find some way to improve their state of mind. Different individuals find different solutions. Some cats devote their attention to other self-rewarding behaviours such as eating, with consequences soon visible in their waistline. Others become passive. Some individuals find it easier to adapt to indoor life than others. All in all, sufficiently attractive substitutes to prey appear to be at least as important to the well-being of adult cats as actual play is to kittens.

Sliding and acrobatics

At any given moment throughout the forests and oceans of the world, the vast majority of animals engaged in play are young individuals. Pups, cubs, fawns, fledglings and so on. Among some species, however, even mature adults join in the fun.

In a riverside scene blanketed with midwinter snow, an otter is bounding vigorously uphill. On the top of the riverbank, he suddenly makes an agile U-turn and throws himself down on the snow. A couple of kicks with his hind feet send him sliding all the way down. At the bottom of the bank his sleek figure emerges from the snow. Again the otter runs uphill with its characteristic bobbing gait. Further along the frozen river, two more otters are similarly busy on the flat, snow-covered ice. After running starts, a kick of their hind feet sets them off sliding on their stomachs for several metres. They sometimes take turns, or both perform slides in unison.

The sliding habits of otters are well-known among zoologists and naturalists, but for a long time they were assumed to simply be a way to save energy while getting from A to B. That may well be part of the story too, but systematic observation of otters in the wild has shown that they often go sliding just for the sake of it. In a number of documented cases the otters were clearly not going anywhere, but just repeatedly climbing up the same bank and sliding down again.

Seals, too, retain their playfulness into adulthood, frequently swinging and wheeling around underwater. This apparently purposeless acrobatic behaviour occurs both in the wild and in captivity, but takes more varied forms in the wild.

Herring gulls for their part often repeatedly carry sticks or empty shells up into the air, drop them, and then swoop to catch them in mid-air. Parrots entice familiar individuals into mock pursuit, and ravens play with objects together. Ravens also slide down rooftops and mounds of snow, sometimes on their backs and sometimes on their stomachs, or they may hang from power lines by their bills or somersault round branches. The list goes on. Even though the number of species in which adults continue to play constitutes a minority within the whole animal kingdom, there are hundreds of such species.

The most playful bird in the world is the kea, a species of parrot that lives in mountainous parts of New Zealand. Keas’ behaviour meets the scientists’ five criteria for genuine play so well that many a local resident wishes they would not. Keas’ destructive habits include breaking TV aerials, stripping the rubber from cars’ windscreen wipers, and biting off the air valves of car tyres. Such activities are most common among juvenile keas, but adults also get up to similar tricks. Shoes left outside can swiftly have their shoelaces pulled out, and many a pair of sunglasses has been snapped up by an inquisitive beak and never seen again. On one occasion a kea was observed happily dragging away a two-kilogram camping axe. Keas have also been seen rolling up a door mat and pushing it down the stairs, and absorbedly throwing stones into water for long periods. Researchers have concluded that this behaviour is genuine, self-rewarding play, because keas do not get any obvious benefits from all the energy they put into such endeavours. Even when they destroying tents or campers’ clothes, they do not utilize the resulting shreds for such purposes as nest material.

The minds of keas fascinate scientists for other reasons too. Their versatile learning skills are particularly interesting. Though we cannot know exactly what it feels like to live as a kea, we can at least safely guess that it feels very different to being an animal with no sense of play.

Some species have never been observed to play. In his book The Genesis of Animal Play, Gordon Burghardt counts the number of orders among mammals and birds in which play has been reliably been documented in at least some species. Orders are large groups of related species. Mammals are most often divided into 28 orders, such as whales, bats or carnivores of which 20 orders include species that have been confirmed to engage in real play.

The most diverse forms of play behaviour have been found among whales, seals, elephants, carnivores and primates, including us humans. At the other end of the scale, there are a few mammalian orders among whom no play behaviour has ever been observed. These include the colugos, aardvarks and three poorly studied marsupial orders: shrew opossums, monito del montes, and marsupial moles. Among bats and the egg-laying mammals (echidnas and platypuses), something resembling play has been observed, though scientists remain unsure of its exact significance.

Among birds, play has been observed in 14 of the 28 bird orders. The playful orders include woodpeckers, owls, pigeons, parrots, galliformes (such as chickens, grouse and quails), anseriformes (such as ducks, geese and swans), and the most numerous bird order of all, the passerines, which includes ravens and other corvids. The list is far from closed though. New field observations on animal behaviour continue to accumulate, and they may yet reveal the existence of play in some of the orders we still think of as entirely serious.

Intelligence has surprisingly little to do with mammalian or avian playfulness. After calculating how much time individuals of the most intelligent species spend playing on average comparing to the others, there seems to be no difference. However, in terms of what the animals do during their play, clear differences emerge. More intelligent animals have more complex forms of play. There also is some overlap between the animals with the highest intelligence and those with the most frequent adult play. Both of these categories include dolphins, us primates, corvids and parrots.

What makes an animal want to play?

If play really is prevalent in so many animals from ravens to rodents, the obvious question is: why? The classical answer is that they are practising skills they will need later in life. At first glance, this makes sense. Animals’ play often involves the same skills the species need to thrive in the wild. Among wallabies, for instance, the playful fights of juvenile males consist of similar moves to those used by adult males fighting over females, though the juveniles substitute serious kicks with harmless hopping. Some scientists think that play may result in even more important outcomes than better-developed muscles and motor coordination. The Czech ethologist Marek Špinka of the University of Prague has spent decades studying play in animals from pigs and cattle to monkeys. He thinks one of the key benefits is “training for the unexpected” – training the mind, not only the body. While playing, an animal learns to operate in rapidly changing circumstances. At one moment, it has the situation under control, but seconds later the stone may fall off its paws, or its sibling may pounce from an unexpected direction. Animals who enjoy such unpredictable but safe physical exertions can improve by practice their attentiveness and their ability to react flexibly.

The rat-tickling Jaak Panksepp and his colleague Stephen Siviy have found that play directly affects the brain development of young animals. During play, many parts of the brain are activated simultaneously. This strengthens the neural connections between them, and helps to build new connections, including some between areas that would otherwise be unconnected. Studies of the brains of humans and animals alike indicate that having a vast number of such connections is one of the real keys to an efficiently functioning brain. The larger the network between separate areas of the brain, the better the person or animal will perform in creative problem-solving and other tasks in which they need to assemble seemingly disparate bits of information to form a functioning solution.

It is little wonder that natural selection has favoured playfulness in the evolution of many animals. This does not, however, explain why play exists in the first place. If we could go far back enough in time, to the point in prehistory when some long-extinct animal performed the first ever playful hop or nudge, we would still have to ask: why? No animal before that had been able to derive the benefits of practice from play. So there was no way that natural selection could have established play behaviour in its evolution. Future benefits to come could not have been the reason for some ancient animal to engage in the first-ever fit of playfulness.

Gordon Burghardt and many other scientists think that the reason why play first emerged among prehistoric animals was probably the simplest and most obvious one. It was fun. When an animal is engaged in fulfilling one of its behavioural needs – which certainly already did exist, and had been honed by countless millions of years of evolution in foraging and other vital behaviours – such an activity in itself is experienced as rewarding. This is because an intense internal motivation for crucial behaviours is an asset strongly favoured by natural selection. A carnivore following potential prey, or a bird turning over dry leaves on the ground in search of worms and maggots, experiences a surge of dopamine and other relevant neurotransmitters in its brain. This results in a positive experience that we humans would in ourselves call a good feeling. The basic motor patterns for such behaviours, including those in this prehistoric pioneer of playful behaviour, are for the most part genetically hard-wired. In the brain of a newborn animal, most of them are not active yet, but later the necessary neural connections begin to grow, and the relevant genes get switched on. At this point, something new emerges in the youngster’s mind. A rabbit pup feels an urge to leap and bounce. A kitten finds small and moving objects fascinating to chase. The young animals start to indulge in these passions using their nascent physical abilities. They are clumsy at first, but these behaviours nevertheless activate the same neurotransmitter pathways that will later reward the adult animal for its fully formed performance. From a pup or a kitten’s point of view, pouncing or chasing feels good. So they do it again and again.

It is entirely possible that even today every individual animal discovers the joys of play in this same way: entirely by themselves. The only difference between the first prehistoric animal players and modern animals is that by now there have been millions of years of natural selection favouring those who do play, because they consequently reap the benefits of improving their skills. For this reason, modern species exhibit much more complex forms of play than our distant ancestors would have.

Do different kinds of play feel different?

Researchers often define three categories of animal play: object play, locomotor play and social play. Each of these types of play may have evolved separately. Object play may have its origins in foraging behaviour, which in many species involves the manipulation of various objects. Object play is indeed most common in animals whose adult lives involve difficult forms of object manipulation, such as birds of prey and predatory mammals. Locomotor play may be derived from an even more basic part of life: a young animal experimenting with the postures and movements that are hard-wired in its brain by the genes inherited from its parents. Most inborn postures and movements don’t feature in the actual behaviour of the animal from birth, but instead they start emerging at specific ages. The appearance of such novel urges may seem as surprising to the young animal itself as it does to an onlooker, warranting some experimentation that can give rise to play.

For social play, scientists have suggested several possible root causes. Social play might emerge from an animal’s first attempts at predatory behaviour, or sexual behaviour, or movements of the kind that will later be needed for serious fights with animals of the same species. In some species, social play may be derived from just one of these behavioural aspects, while in other animals it seems to involve various combinations.

In many ways the question “What’s it like to be an animal?” has different answers depending on the kind of animal we are talking about. Different types of play in different animals can give us many clues to animals’ experiences. But we can safely make an educated guess that a deer fawn prancing around feels something quite different from a young crow absorbed in manipulating pebbles with its beak.

This idea of animal play as an umbrella concept covering three distinct forms of behaviour and experience gains further support from the finding that many groups of animals do not exhibit all three types of play. Ducks and geese have only ever been observed engaging in locomotor play. Pigeons only play with objects. Hyraxes – small African mammals that look a bit like oversized guinea pigs, but are actually related to elephants – only practice social play, with no locomotor or object-oriented elements. Among animals that exhibit more than one type of play, the experimental nature of play often results in combinations. Behaviour observed in litters of wild boar piglets provides a good example of this. One of the striped piglets picks up a stick with his teeth and waves it around. Object play: check. Still carrying the stick, he starts to dash back and forth. Locomotor play: check. A few of his littermates are meanwhile rooting about nearby. The piglet then dashes in front of them, before suddenly turning and scampering away. His attempt is successful: the other piglets stop searching for grubs and chase after him, trying to grab the stick. Social play: check.

Even among animals who combine distinct play types in a single bout of play, inherent differences between play types may be revealed in other ways. During the development of young animals they may appear at different times, for instance. Hyena cubs start engaging in social play during their second week of life, shortly before their mother carries them from her own den to the communal den of the whole hyena clan. During the following week, the still very small cubs realize that it is also possible to entertain yourself by simply experimenting with the movements you can do with your own body. This gives rise to a range of hops and wobbly sprints. During their fourth week, hyena cubs develop an interest in bone shards, strips of skin and anything else they can bite and drag around.

The fact that different components of play emerge at different ages has dramatic consequences for a growing animal’s perceptions. They may alter the meanings it will associate with other animals and with elements of its environment for the rest of its life. This is because whenever a new sensation or interest arises in a cub’s young and still rapidly developing mind, it gets intertwined or merged with the other behaviours and perceptions the cub already has. During this phase the kinds of species-specific behaviours that are genetically hard-wired, but have not yet emerged at this age, have no chance of getting entangled with this newfound interest.

Such effects are especially profound when the brain is receptive to the development of a specific behaviour during a limited window of time. In dogs, for example, the majority of social behaviours form when a puppy is between one and four months old. Professor Raymond Coppinger of Hampshire College in the US, who has decades of experience studying the behaviour of dogs and wolves, has shown how this explains why different breeds of dogs play different games. He gives an example concerning two types of dogs that have been used by shepherds in various parts of the world for centuries: herding dogs and livestock-guarding dogs. Herding dogs, such as border collies, are fast, agile dogs able to move sheep from one place to another. Livestock-guarding dogs, such as the Pyrenean mountain dog, are massive and robust. They live among the sheep from early puppyhood onwards, and their sole function is to deter wolves and other predators from attacking sheep by their presence.

Herding dogs are trained to recognize and follow the shepherd’s commands, but their enthusiasm to work stems from a trait inherited from their wolf ancestors: a fascination with following potential prey. When selecting the best herding dogs to breed, shepherds have necessarily favoured those with a keen interest in following and chasing anything that moves. This behaviour has its onset at an early age, when social behaviours are still being formed in puppies’ developing brains. Livestock-guarding dogs, contrastingly, should not chase sheep – at least not in their owners’ opinion. So shepherds have usually got rid of any livestock-guarding dogs that indulged in such undesirable behaviour, thus preventing them from passing on their genes to subsequent generations. This has resulted in breeds of livestock-guarding dogs with a weak or non-existent innate interest in chasing moving targets. For puppies with herding-dog genes, it is easy to discover that the newfound joys of chasing can also be turned into a social activity: play-chasing each other. When the attraction of moving targets first crosses a puppy’s mind, its brain still is open for new types of social interaction to form. Livestock-guarding dogs, on the other hand, have already largely completed the development of their social behaviour by the first time they are able to feel an interest in running after something.

Extra energy increases playfulness

The following situation may be familiar to anyone who has owned a puppy dog. The puppy meets some other pups of a similar age out in the park. At first, all goes well. The puppies seem to play happily, creating a whirlwind of soft bounces and wagging tails. But gradually the mood starts deteriorating. One of the puppies suddenly growls in earnest; then another. The soft play-bites are not so soft any more. Little by little it starts looking like a serious fight. A wise owner will have interrupted the puppies by now, asking other owners to each soothe and calm down their own puppies. The whole affair feels rather puzzling though. After all, in the beginning it looked like the puppies genuinely wanted to play; but in the end they became genuinely aggressive.

The change in the puppies’ state of mind is due to one of the constraints on play. Usually, though not always, animals are only capable of playful mood when they have extra energy. In the beginning of the puppies’ encounter in the park, there was plenty of energy to spare. But the longer the rough-and-tumble lasted, the more tired the puppies grew, and this drained an essential part of their motivation to play. As their playfulness faded away, all that remained was the mood and the behaviour that play fighting serves as a modified form of: real fighting.

This is not the whole story, however. Part of the reason for such turns of events lies in skills that the puppies have not yet had an opportunity to learn. In the wild, cubs of any species spend all their time with their siblings. This gives them ample opportunity to learn how to stop situations getting too boisterous; essentially, when to stop. Pet dogs are weaned early from their mothers, often before the age of two months, after which they usually spend most of their time isolated from other puppies, who they may only meet a couple of times a day at the most. This is why some puppies get carried away: they have had fewer opportunities than wild animals to practice self-control during play.

Puppy dogs are not the only ones to forget about playfulness when they become fatigued. Surplus energy seems to be one of the most crucial prerequisites for a playful mood throughout the animal kingdom.

Animals of different species differ enormously in how much of their time they spend playing. As we have seen, the dividing line does not follow differences in intelligence. Instead, the extent of play clearly correlates with how easy it is to find enough food. The tighter the energy budget that an animal has to live with, the less inclined it is to devote energy to such an extravagance as play.

The quest to secure sufficient energy is more challenging for small animals than large ones. Animals mainly lose body heat from their external surfaces, and the ratio of an animal’s surface area to its body volume increases as the size of the animal diminishes. This is the main reason why small animals have to eat proportionately more than large ones in order to maintain their body temperature. Tiny shrews and bats have been observed to play very seldom, if at all. Elephants, on the other hand, easily get into the mood for fun, especially when there is an abundance of resources, such as when they arrive at a river to drink.

The crucial role of energy efficiency in playfulness also crops up in another correlation. Swimming requires less energy than any other form of locomotion. Aquatic animals also are far more playful than their land-based counterparts. When carrying out comparisons within mammalian orders, the most playful species are usually found in the water. Few rodents exhibit play behaviour as frequently as beavers, for example. Among carnivores, the same is true of otters.

Does this mean that life is somehow more fun if you happen to be born as a large animal or an aquatic animal? Is it especially delightful to be a whale, at least in waters where there is no whaling? The current body of scientific evidence provides no definitive answer to this question, but it is quite possible that “yes” would be the correct guess. Play stems from abundant energy. It occurs only when an animal is not suffering from hunger, and in the absence of direct threats. It is therefore often an indication that all is well at the moment. But there is more. In addition to growing out of well-being, play positively creates still more well-being by activating neurotransmitters that generate a sense of pleasure.

A link between an animal’s energy budget and a playful state of mind has also been found at the level of the individual. One such experiment was carried out on wild meerkats. Meerkats are certainly not large, or aquatic. These lithe ground-dwellers weigh less than a kilogram and live in an arid environment, where they have to work hard to find enough grubs and millipedes to eat. Their behaviour in the wild has been subject to a long-running research programme, the Kalahari Meerkat Project in South Africa, led for over 20 years by Professor Timothy Clutton-Brock of the University of Cambridge. Generations of meerkats have become habituated to the presence of researchers, to the extent that the meerkats now go about their daily business right in front of the researchers’ noses, peacefully sunning themselves after a chilly desert night, or in the midst of a frenzied scorpion hunt. Should the need arise to find a bit higher vantage point, it is not uncommon for a meerkat to jump onto the shoulder of a nearby scientist.

Most of this research programme is based on observing the meerkats, but Clutton-Brock and his research team also carry out occasional experiments. These are planned carefully to ensure they cause no harm to the meerkats. In one of these experiments, they gave half of the pups in each litter a piece of boiled egg twice a day for a few weeks. To keep the other pups from snatching the goodies, the extra food was served on a tray onto which the pup had to climb. The tray was then lifted, with the pup and all, to ensure he could eat free from competition. Once the pup had finished, the tray was lowered back onto the ground. Behavioural observations revealed that this extra feeding did result in an increase in playfulness – specifically in those individuals that had got the extra boost of energy. Several other experiments have similarly shown that the abundance of resources does affect the motivation to play. The meerkat experiment also nicely illustrates how it is possible to carry out experimental research on animal behaviour and motivations without a laboratory environment or procedures that are stressful to the animal.

Does playfulness equal happiness?

The familiar playfulness of dogs has a precedent in their ancestors. Wolves retain their ability to play well into adulthood. Yet something has changed. It often happens that when a species of animal is kept by humans for centuries or millennia, its inherent playfulness increases. For example, pet rats and lab rats play the same types of games as wild rats, but they play them more frequently, especially when it comes to wrestling games.

Increased playfulness is one aspect of a phenomenon called domestication. Domestication is a result of the genetic, heritable changes that take place when animals are kept in captivity for dozens or hundreds of generation and subjected to selective breeding. Typical effects of domestication include a smaller brain size, reaching sexual maturity at an earlier age, and a reduction in the so-called flight distance, which is the distance at which an animal flees from an approaching potential threat.

Pigs and other farm animals are usually given enough food. So their energy budget should be fine, setting no constraints to play. They also are domesticated, so are inclined to frolic more than their wild ancestors. Yet observations of pigs in ordinary modern-day farms lead to a puzzling conclusion. Piglets do engage in scampering about and chasing during their first weeks of life, just like their wild counterparts. But soon after that their playfulness starts to fade away. By the age of two months, farmed piglets turn strangely serious, exhibiting only rare and short bouts of play. Exceptions to this are pigs on those few farms that have outdoor runs where pigs can behave more experimentally and actively. Since these pigs are often of the same genetic stock as those kept in intensive farms, the reason for the early disappearance of play has to be their environment rather than something inherent in the pigs.

The Czech researcher Marek Špinka and his research group at the University of Prague have found that a reduction in the play behaviour of piglets correlates with more serious behavioural problems. In most pig farms today the floors of the pig pens are bare concrete or plastic, with no straw or other loose material. When the Czech researchers experimentally gave piglets some straw on the floor for the first weeks of their life, they noted a significant increase in play behaviour. Observing the same individuals a few months later showed that their social behaviour had also benefited from the addition of some natural materials to their pens. The pigs were less aggressive towards each other at the food trough than a control group reared in an ordinary bare pen.

The extent of play behaviour is often brought up as a promising indicator when scientists seek objective ways to measure how animals actually fare in various man-made environments. Stress and fear as experienced by animals are often difficult to recognize, even for professionals such as farmers and inspectors. This is partly because a common symptom of stress or fear is for an animal to stay quiet and seemingly do nothing, and partly because farmers and inspectors seldom get an opportunity to observe the behaviour of animals of the same species in a more natural environment. This means that they lack anything to compare the farmed animals’ behaviours with.

Some welfare measurement systems have been defined for farm animals, mostly based on ratings of their environment. One of the currently ongoing research activities in the field of animal welfare science involves developing animal-centred measures which would improve the accuracy of welfare assessments, especially on the individual level. On farms housing large numbers of animals, animal welfare is most often discussed in terms of physical structures and animals’ average survival rates. To get a better idea of how the animals are faring, scientists have recognized a need to develop better methods to detect problems that do not manifest themselves in such drastic outcomes as increased mortality or severe injury rates. The question as to whether measures of playful behaviour could serve for such a purpose stems from the idea that if animals consistently play significantly less than would be normal for their age and species, this may indicate the animals are experiencing chronic stress or fear.

Together with his colleague Suzanne Held of Bristol University, Špinka has further examined what would have to be taken into account if play behaviour were to be utilized in animal welfare assessments. They point out that whereas the general idea – that reduced play often does signal poorer welfare – is correct, there are a few exceptions that need to be factored in. One of them is the so-called rebound effect. When an animal is released from a long-lasting frustrating situation, it can react with an outburst of exhilaration.

Playing further in the family tree

Outside the realms of mammals and birds, confirmed cases of genuine play are rare. Scientists currently have no sound evidence of the existence of play among amphibians, although a few researchers have made intriguing observations on tadpole behaviour that warrant further research. On the other hand, reptiles neatly follow the rule of energy budgets. Play behaviour has been recorded in a few reptilian species, all of which are either large, aquatic, or both.

One of the largest reptiles in the world is the Komodo dragon. This is a species of monitor lizard whose heftiest individuals weigh in at over one hundred kilograms and grow to a body length of three metres. Playful behaviour among Komodo dragons has been studied and filmed in several zoos. The dragons only exhibit one of the three types of play described above: object play. In practical terms this means pushing around buckets and shovels, snatching handkerchiefs and notebooks from keepers’ pockets, and inventing a number of uses for old shoes. Individual dragons differ in their preferences. One of the dragons observed at the National Zoological Park in Washington DC favoured a frisbee, spending more time playing with it than with all the other toys combined. The dragons found multiple uses for a range of objects from shoes to hula hoops, which could be carried, shaken or worn around a reptilian head. Unlike the focused behaviour typically seen when adult cats prey on a toy, the dragons’ undertakings were so varied that even when critically scrutinised they still fulfilled all the five criteria for genuine play.

Most other observations of playful reptiles concern aquatic turtles. The National Zoological Park in Washington DC also used to have a large male Nile soft-shelled turtle. These turtles are almost as heavy as a Komodo dragon, though their bodies are a lot shorter and more rounded. This individual had trouble adapting to captivity. He kept raking his foreclaws in the flesh of his neck and biting his forelimbs, causing considerable damage to himself. To distract him from this self-mutilation, the zookeepers started giving him objects such as a rubber hoop and a basketball. This intervention succeeded beyond all expectations. The turtle dropped most of his self-harming behaviour and busied himself with object interaction. His favourites were a piece of rubber hose and a hoop made of rubber hose and half-filled with water so that it floated vertically underwater. The turtle used these toys for biting, shaking and pushing around. Occasionally he also swam through the hoop, sometimes several times in succession. Gordon Burghardt’s research group filmed him on video for three days and made a careful analysis of the footage. The turtle’s behaviour fully met the criteria for actual play, but the most surprising finding concerned the sheer amount of time he spent toying with these objects: one fifth of the total time he was observed, which is quite a high figure for any animal.

Anyone who has followed the recent surge of research findings on the cognitive abilities of fish will not be surprised to learn that fish feature more heavily than reptiles on the list of confirmed cases of play behaviour. Activities meeting all the criteria for play have been found in salmonids, cichlids, sharks and several other groups. Among the fish groups that have especially attracted the interest of scientists studying play are the mormyrids. These African fish have unusually large brains. The ratio of brain size to body size is approximately the same in mormyrids and in humans.

Research on play behaviour in mormyrids began in the 1950s. One of the scientists most involved was Monica Meyer-Holzapfel, Director of the Dählhölzli Zoo in Bern, Switzerland, and an Honorary Professor of the University of Bern. She conducted observations of her zoo’s elephant-snout fish for a period of seven years, and also collected information from German and Danish colleagues. The elephant-snouts’ favourite activity involved balancing small stones, snails and other objects on their snouts. When playing with twigs, they favoured short, forked twigs with three prongs, as they were far easier to balance than simple twigs. If an object did fall, the fish would often quickly swim beneath it to catch it before it reached the aquarium floor, and resume their self-invented circus act.

Meyer-Holzapfel carefully examined potential explanations. Could this be part of the species’ natural feeding behaviour redirected to other targets, as has been observed in some animals in captivity? This was considered unlikely, because the movements of the fish did not bear much resemblance to the actual feeding behaviour of the species. Maybe the fish had parasites on their snouts, and were trying to rub them off? On the other hand, the fish were never seen to scratch their snouts against any objects. When one of the fish actually did develop a parasitic fungus infection, it stopped playing completely and just lay on the bottom of the aquarium, rubbing its side on the floor. Could this behaviour be a kind of courtship display perhaps, evolved to advertise the individual’s fitness to the opposite sex? This did not seem likely either, as the fish performed their balancing tricks with equal vigour all year round, not just during the breeding season. After discounting all these other possible explanations there was only one option left.

If the motivation for an individual animal to play is a pleasant feeling that results from the activity, this strongly suggests that reptiles and fish engaging in playful behaviour are capable of feeling pleasure. For experts in the behaviour of these animals, this comes as no surprise. If experts were asked to name the group of animals on which the widespread public perception differs most from the interpretations of scientists specialized in analysing their behaviour, the most likely candidates would be “cold-blooded” animals such as reptiles and fish. As we have seen in other chapters of this book, several discoveries have been made in recent decades indicating that reptiles and fish possess characteristics previously thought to be the sole preserve of the “higher” animals.

While the existence of play in some species supports the conclusion that a sensation of pleasure or fun does exist in their minds, the absence of play behaviour in other species does not mean they are doomed to a life without pleasure. The non-players may simply not have enough extra energy to be able to afford to play. Reptiles and fish are ectotherms, dependent on external heat sources such as sunlight or water temperature to keep their bodies within a suitable temperature range. They usually have to live on a considerably tighter energy budget compared to us endotherms – mammals and birds – who can convert food into body heat. This may be the most important reason why playing is so much more common among endotherms than among ectotherms.

So far, all of the animals we have examined are vertebrates – animals with backbones, our nearest evolutionary relatives. Climbing onto more remote branches of our family tree, we enter the enormous and diverse realm of invertebrates. It is generally assumed to be a world without play, and it may mostly be, but very little research has been conducted to show how strictly true this assumption might be. The only group of invertebrates where serious research into play has been conducted are the cephalopods: octopuses, squids and cuttlefish.

Michael Kuba of the Konrad Lorenz Institute in Austria is one of the scientists researching cephalopod behaviour and cognition. In his play experiments he has used the most commonly studied species of octopus, the aptly named common octopus, which in the wild lives in the Atlantic and the Mediterranean. In his aquarium studies Koba provided the animals with novel objects made of Lego blocks. Two types of objects were used: a simple cube, and a more complex snowflake-like structure designed to have maximal rough surface suitable for grasping with tentacles.

Individual differences soon emerged. Nine out of the 14 octopuses started experimenting with the objects. They explored them with their tentacles, pushing and pulling them in various directions, and passing them from one tentacle to another. One observed activity involved transporting the object along the water surface by holding onto it with one or more tentacles while using the other tentacles for swimming. For the purposes of comparison, the researchers dropped food items into the tanks. These were not played with, but promptly eaten instead. The octopuses interacted with the Lego structures as frequently after feeding as before their meals, excluding the possibility that the reason for manipulating the objects could have been the hungry animals checking whether there was any food in them. The most complex bouts of activity simultaneously fulfilled all five criteria for play, so Kuba and his team concluded that octopuses do engage in actual play behaviour.

Does this mean that even these strange blobs of jelly can have fun? At present, we know little about the kinds of experiences invertebrates may enjoy. These octopian studies nevertheless illustrate how researchers keep making surprising new discoveries in this field. It can safely be predicted that in future we will surely continue to get ever more enticing glimpses of the inner worlds of creatures very different from ourselves.


 

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