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Playful fun in dogs

2015; Elsevier BV; Volume: 25; Issue: 1 Linguagem: Inglês

10.1016/j.cub.2014.09.007

1879-0445

Marc Bekoff,

Evolutionary Game Theory and Cooperation

A shaggy brown terrier approaches a large chocolate Labrador in a city park. When the terrier gets close, he adopts a yoga-like pose, crouching on his forepaws and hiking his butt into the air. The Lab gives an excited bark, and soon the two dogs are somersaulting and tugging on each other's ears. Then the terrier takes off and the Lab gives chase, his tail wagging wildly. When the two meet once more, the whole thing begins again. (Grimm, 2014Grimm, D. (2014). The Canine Code. Washington Post, 20 May. http://www.washingtonpost.com/national/health-science/in-dogs-play-researchers-see-honesty-and-deceit-perhaps-something-like-morality/2014/05/19/d8367214-ccb3-11e3-95f7-7ecdde72d2ea_story.htmlGoogle Scholar) Why study play and fun in dogs and their wild relatives? Clearly, these two dogs are having fun. Domesticated dogs are fascinating mammals. We created them in our own image, often favoring traits that compromise their health and longevity, and they also vary greatly in size, shape, mass, color, coat, personality, and behavior. And, because they are easy to observe and to identify reliably in various environments, dogs are wonderful subjects for studying a wide variety of behaviors, including social play. So too are wolves and coyotes. Through comparative research, we have learned much about the nitty-gritty details of what dogs, wolves, and coyotes do when they play and how they have fun (for example, how they ask another dog to play, how they announce their intentions, how cheaters are treated, and how they apologize and forgive transgressions against the rules of fair play). We also have generated some theories about the evolution of social behavior and moral sentiments — wild justice — and have begun to answer 'big' questions about such areas as fairness, peace, moral behavior, and social justice in animals. Having fun on the run and playing fairly is tightly linked to the evolution of social tolerance, social reciprocity, individual fitness, and peaceful relationships among group-living animals. What I write here for dogs, wolves, and coyotes also applies to other animals. What is play? In the late 1970s, John Byers and I developed a well-received definition of the word 'play' as it applies to social interactions, namely: "social play is an activity directed toward another individual in which actions from other contexts are used in modified forms and in altered sequences". Our definition centers on what animals do when they play — how they use a kaleidoscope of actions such as biting, pouncing, mounting and humping, and body slamming in unpredictable sequences — or on the structure of play, rather than on possible functions of play (Figure 1). Of course, in addition to social play, dogs and other animals engage in self-play such as tail-chasing and object play, including playing with various types of balls or other objects, and tug-a-war with other individuals. Here I will focus on social play and why it is such an important activity. But, both self-play and object play are clearly fun. One reason why studying play has been so difficult is because it is a hodge-podge of lots of different activities borrowed from various social contexts, and it takes a lot of time to learn about the details of this fascinating behavior. It can take many hours to conduct frame-by-frame analyses of as few as ten minutes of play captured on video, and these sorts of analyses are essential to gaining an understanding of this behavioral phenotype. The 'F' word: what is 'fun'? Fun is one of the two 'F' words that have received growing attention by ethologists, the other being 'friends' (researchers ask, for example, do animals make friends?). Ample data show that animals both have fun and make friends. Like play, fun is hard to define, but you know when you're having it. Having fun means doing something that is amusing, enjoyable, and pleasurable and feeling good about it. It is an evolved adaptation and important for keeping an action or activity in an individual's behavioral repertoire. In my studies, I take a strongly evolutionary and ecological approach using Niko Tinbergen's integrative ideas about the questions with which ethological studies should be concerned: namely, evolution, adaptation, causation, and ontogeny (development and the emergence of individual differences). University of Tennessee psychologist Gordon Burghardt, author of The Genesis of Play, later suggested adding 'subjective experience' to Tinbergen's scheme. So, concerning play and fun, we can ask: Why did they evolve? How do they promote survival value and reproductive fitness and allow individuals to come to terms with the social situation in which they find themselves? What causes play and fun? How do play and fun develop? What is the emotional side of play and fun or what is the personal experience of animals while they are playing? Play is serious business but it also is fun: animals seek it out, it is a voluntary activity and play is highly contagious. Playing dogs are magnets for others and I am always amazed at how fast dogs invite strangers into a playgroup and how they are absorbed into the fun. I think it's clear that dogs know when others are having fun and when they're not. And, as an aside, studying play is a lot of fun in and of itself: research should be fun and I'm sure I've continued to study play for more than four decades because it is fun to do. Why has playful fun evolved? Play may serve a number of functions simultaneously, for example, socialization (allowing animals to become card-carrying members of their species), exercise, practice, cognitive development, or training for the unexpected, the last theory being based on the kaleidoscopic (unpredictable) nature of play sequences. I see part of the fun of playing to be related to its unpredictability and the difficulty of one dog knowing what his or her play partner will do next. Play may also have what is called an 'anxiolytic effect' by reducing anxiety during tense situations and preventing escalation to an aggressive encounter. No matter what the functions of play may be, many researchers believe that it provides important nourishment for brain growth and helps to rewire the brain, increasing the connections between neurons in the cerebral cortex. Clearly this is a vital consequence of play and having play be fun is a good way to be sure animals play. Bows are honest signals: the hidden language of play. My early research focused on the importance of 'bows', a yoga-like position, in the initiation of play. Bows occur when a dog crouches on his forelimbs and sticks his butt into the air, and they send the message "I want to play with you". In my early research, however, I did not see how bows were used to punctuate play sequences and tell others, in essence, "I am going to bite you hard but it is still play" or "I am sorry I just bit you so hard, please forgive me". I also did not see at the time how individual patterns of play could be related to the development of social bonds and individual dispersal patterns or to reproductive output. Subsequent studies show that individual differences in play have widespread and long-term effects. What is the fair way to play and have fun? To gain an understanding of the nature and importance of play and fun, it is essential to do detailed film analyses, because dogs and other animals use subtle signals and very rapid exchanges to maintain the play mood. Hidden in the frivolity is a language of play that includes honesty, empathy, and cooperation. I think of cracking the canine code as canine confidential. When animals play, they are constantly working to understand and follow the rules and to communicate their intentions to play fairly. They fine-tune their behavior on the run, carefully monitoring the behavior of their play partners and paying close attention to infractions of the agreed-upon rules. Four basic aspects of fair play in animals are: ask first; be honest; follow the rules; and admit when you're wrong. When the rules of play are violated and when fairness breaks down, so too does play and the having of fun. For example, when dogs ask another individual to play they use different actions, including bows, pawing, and faking left and going right and running away to initiate chase (not to defend themselves). Following the rules simply means that a dog shouldn't bow if they don't really want to play. Other dogs expect them to play fairly and not try to mate with them or dominate them. And, admitting when you're wrong means that, when a dog bites another dog too hard or slams into them vigorously, she will do an immediate bow as if to say "I was really playing with you, I'm sorry", and the other dog accepts the apology and forgives her and play continues. The main point that has emerged from decades of study is that, while dogs are having 'fun on the run', they are carefully negotiating what is happening and using subtle signals to maintain the play atmosphere. It also turns out that humans do much the same to keep play fair — just watch kids on a playground. What happens when play is not fun anymore, when individuals break rules? Play bows are honest signals, signs of trust. Bows and other play signals are rarely used to deceive others in canids or other species. Although many people think that the rules of play break down frequently, they do not. We learned that on only around 2–5% of time do animals violate the agreed upon play mood. Do dogs or other animals feel shame or guilt when they lie about their intentions to play? We really do not know, but this would be an exciting area of research. We do, however, know that for wild coyotes, individuals who do not play fairly (cheaters) and who reduce the fun factor are actively avoided or their play invitations are ignored and they do not form strong and long-lasting social bonds. Because they are socially ostracized these loners tend to leave their natal (birth) group on their own and suffer almost four times the usual mortality rate during the first year of life. Violating the rules of play is maladaptive and can disrupt the efficient functioning of the group. This is a good example in which the data we collected on social play and the dispersal patterns of identified individuals did not make sense to us at the time: however, as ideas about fair play and individual patterns of dispersal emerged they took on significance. A major message from research on captive and wild canids is clear: don't bow if you don't want to play and have fun. Play means play. Morality of fun: if you're having fun, why not be nice? Social morality, in this case behaving fairly, is an adaptation that is shared by many mammals. Behaving fairly evolved because it helped young animals acquire social and other skills needed as they mature into adults, and because it is adaptive and helps animals, including humans, survive and thrive in particular environments. There is no reason to assume that social morality is unique to humans. And, having fun is a good way to keep fair play in the behavioral repertoire. Animals can have fun, be nice to one another, be fair, and honor the trust that each has for the other. In order to play they have to do just this, because most, if not all, individuals in a group will benefit from adopting this behavioral strategy and group stability may also be fostered. Can dogs and other animals have too much fun? Social play clearly is fun for the players. Future research should also consider whether it is possible for animals to have 'too much fun' or behave 'too fairly', following up on research on humans in the field called 'diagonal psychology' that shows there can be negative consequences associated with being too full of oneself or for being 'too happy' or having 'too much fun'. Thus, one can ask if there is stabilizing selection for fun and fairness that reins in the possible costs of behavior that can be too risky or too costly, including social play. We know, for example, that individual golden marmots, southern fur seals, and young bighorn sheep who are caught up in the frivolity of play seem to suffer more injuries and higher mortality than those who are not playing. So, while there are bits of data that inform this area of inquiry, it really is wide open for further detailed study. What is really nice about studying play and fun in dogs is that you can see all of the above at your local dog park. When we study play and fun we're really studying ourselves as well. And, it's fun to do. It's a win-win for all involved.