Dogs are "in." Hardly a week goes by that a research paper and numerous popular accounts don't appear in the news. This week is no different. First, on the "down" side, we've learned that researchers in some laboratories in the United States often secretively do whatever they want to dogs "in the name of science" in "wasteful, bizarre and deadly experiments" with little to no transparency. Basically, they get away with murder, using taxpayer's money, and no one does anything about it. 

On the "up" side of things, I was so pleased to learn about a study by Claudia Fugazza, Ákos Pogány, and Ádám Miklósi, who work in the Department of Ethology at Eötvös Loránd University in Budapest, Hungary, that was just published in Current Biology. This new and very significant essay is titled, "Recall of Others’ Actions after Incidental Encoding Reveals Episodic-like Memory in Dogs." Needless to say, this study received broad global coverage in mass media. People really do want to know what dogs know. And, here is a video of how the research was conducted. 

Their summary of the important research essay that's available online reads:

The existence of episodic memory in non-human animals is a debated topic that has been investigated using different methodologies that reflect diverse theoretical approaches to its definition. A fundamental feature of episodic memory is recalling after incidental encoding, which can be assessed if the recall test is unexpected [1]. We used a modified version of the “Do as I Do” method [2], relying on dogs’ ability to imitate human actions, to test whether dogs can rely on episodic memory when recalling others’ actions from the past. Dogs were first trained to imitate human actions on command. Next, they were trained to perform a simple training exercise (lying down), irrespective of the previously demonstrated action. This way, we substituted their expectation to be required to imitate with the expectation to be required to lie down. We then tested whether dogs recalled the demonstrated actions by unexpectedly giving them the command to imitate, instead of lying down. Dogs were tested with a short (1 min) and a long (1 hr) retention interval. They were able to recall the demonstrated actions after both intervals; however, their performance declined more with time compared to conditions in which imitation was expected. These findings show that dogs recall past events as complex as human actions even if they do not expect the memory test, providing evidence for episodic-like memory. Dogs offer an ideal model to study episodic memory in non-human species, and this methodological approach allows investigating memory of complex, context-rich events.

Didn't we already know dogs had great memories?: A brief interview with Dr. Ádám Miklósi

Many animals spend a lot of time resting, often peering around at their surroundings and taking in the sights, sounds, and smells. Dogs surely do this. I often smiled as I watched the dogs with whom I shared my home just hanging out and looking around at their dog and human friends and their environs. When I've done field work on a number of different animals, I also noted that they spent a lot of time just hanging out and looking around as they rested. I was convinced that they were picking up a lot of information from just looking around, and that what they learned they could use in their social encounters with others. 

In response to this new study I received a number of emails asking something like, "Didn't we already know that dogs had great memories?" Yes, we did, and a good deal of "citizen science" shows this to be so. But, I wanted to know more, so I sent dog expert Dr. Ádám Miklósi, founder of the Family dog Project who was involved in the study, two questions to which he responded immediately. They were, "Why did you do this study?" and "How does it extend what we know from (i) other formal studies and (ii) what people know from watching their dog at home or at a dog park?"

Dr. Miklósi answered the first question quite easily: "Claudia [lead author of the study, Claudia Fugazza] went to a conference on memory, and then she suggested that maybe the 'Do as I Do' method offers a way to provide some evidence for this."

Dr. Miklósi's answer to the second question, "How does it extend what we know from (i) other formal studies and (ii) what people know from watching their dog at home or at a dog park?" was: "As usual this is something that dog people may have assumed the dog is capable of doing. But most of them did not think about the possibility that dogs remember specific events happening around them. This study shows now that dogs (and probably many other animals) are able to do this. So they not only remember (spontaneously) what they have done (there are studies on chimps, rats, dolphins along this lines), but also what their owner did. For example, they may watch the owner cut the roses in the garden one day, and then when they see those flowers again, this memory could pop up in their mind. This could happen without showing any change in behavior, because this is just a spontaneous 'thought,' although in some other cases such thoughts may actually become causes of (spontaneous) behaviour."

In one interview I did about this study, I noted, "Dogs have great memories of a lot of events and this study shows that we’re still learning just how good their memory really is ... Dogs need to be able to learn and remember what their human wants them to do, and there won’t always be an immediate association of the events in time ... So, it is not surprising to me that dogs can remember the ‘Do it’ request after a period of time even if they weren’t expecting to be asked to do something.”

A few of the dogs with whom I lived acted like "know-it-alls": Dogs remember yesterday and much more

This new research reminded me that many of the dogs with whom I lived acted like "know-it-alls." They seemed to have a sense of knowing what I was going to do or what I wanted them to do, although I'd never explicitly taught them to make these associations. I felt the same about some of the wild coyotes I studied for years. They just seemed to know what others were thinking, feeling, and wanted them to do. I'm sure the dogs and coyotes (and many other animals) had some sort of "theory of mind." (See "Theory of Mind and Play: Ape Exceptionalism Is Too Narrow.")

As I read through this new research paper I remembered an essay I wrote last year called "Dogs Don't Remember Yesterday, Claims Psychologist," about the seemingly ludicrous claim that "dogs don't remember what happened yesterday and don't plan for tomorrow." The author claimed that dogs are stuck in an "eternal present." 

In my essay I wrote, "There are many examples of dogs and other animals 'remembering yesterday.' Think of dogs and other animals who have been severely abused and who suffer from severe fear or depression for years on end, and also, for example, think of dogs who remember where they and others peed and pooped, dogs who remember where their friends and foes live, dogs who change their behavior based on what they learned in various sorts of learning experiments, and dogs who remember where they're fed and where they've cached food and other objects. The list goes on and on."

I also wrote, "From an evolutionary point of view it would be somewhat odd and exceptional if mammals such as dogs and many other animals didn't remember yesterday and plan accordingly." Along these lines, the authors of the present study write, "This is the first evidence of episodic-like memory of others’ actions in a non-human species, and it is the first report of this type of memory in dogs. We suggest that dogs might provide a new non-human animal model to study the complexity of incidental encoding of context-rich events, especially because of their evolutionary and developmental advantage to live in human social groups."

This is a very exciting time for the comparative study of animal minds

I'm very pleased to share the results of the present study with you. Yes, many of us already "knew" from "citizen science" that dogs often know more than we give them credit for, but it's also nice to know that science backs us up. I've learned an incredible amount from people writing to me and talking with me about their dogs, and I've often noted that when the serious science is done, results rarely conflict with what many others already knew.

This is a very exciting time for the comparative study of animal minds, a branch of science called cognitive ethology. Please stay tuned for more on the fascinating and "surprising" cognitive lives of dogs and other animals. 

Marc Bekoff’s latest books are Jasper’s Story: Saving Moon Bears (with Jill Robinson), Ignoring Nature No More: The Case for Compassionate Conservation, Why Dogs Hump and Bees Get Depressed: The Fascinating Science of Animal Intelligence, Emotions, Friendship, and Conservation, Rewilding Our Hearts: Building Pathways of Compassion and Coexistence, and The Jane Effect: Celebrating Jane Goodall (edited with Dale Peterson). The Animals’ Agenda: Freedom, Compassion, and Coexistence in the Human Age (with Jessica Pierce) will be published in early 2017.

This story was originally published by psychologytoday.com. Reprinted with permission.

Watching dogs play is very exciting, and there has been a lot empirical research on how and why dogs (and other animals) engage in this activity with boundless zeal. A number of people have asked me to comment about dog play after reading this section in a new book by Raymond Coppinger and Mark Feinstein called How Dogs Work. So, I decided to do so.

The authors begin their chapter 9 on play by claiming, “Hundreds of scientific papers have been written on the subject of ‘play’ behavior—an activity for which dogs are, of course, famous.” Recognizing that there is a solid and growing literature on play—there’s really no reason to put the word play in square quotes—I assumed that what followed would be a detailed review of this research, but rather, what I discovered was a disjointed discussion of play and not an in-depth review of the scientific literature. Instead, the authors offer their own unpublished observations and the results of unpublished student projects, all of which are impossible to assess. 

Do dogs and other animals actually play? Coppinger and Feinstein write that they put the word play in scare quotes because “in spite of the fact that people feel like they know it when they see it, it’s not at all obvious that play is a unitary ‘thing-in-itself’ that can easily be characterized, let alone explained in evolutionary terms.” No one I know who has spent years studying play would argue that play is a “unitary ‘thing-in-itself’,” nor would they agree that play cannot be explained “in evolutionary terms.” Indeed, some of the references the authors include show there are a number of highly plausible evolutionary explanations (and the University of Tennessee’s Gordon Burghardt, who has studied comparative aspects of play for many years and wrote The Genesis of Animal Play, provided the Foreword for Coppinger and Feinstein’s book). 

Why do animals play? Briefly, various theories have been offered about why animals play, and there’s no one explanation that fits all examples of animal play. Detailed comparative data show play is important in social development, physical development, and cognitive development. And, neurobiological research strongly suggests play can be pleasurable and fun and animals may simply play because it feels good, “for the hell of it.” Indeed, many researchers are taking fun seriously, and the 25th anniversary issue of the journal Current Biology was devoted to the biology of fun with many play researchers weighing in on the topic. Coppinger and Feinstein write, “We agree that there is good reason to believe that animals derive pleasure from play - indeed they do from all of their motor activities.” (my emphasis) While animals might derive pleasure from play, eating, and sex, it’s difficult to argue they feel good running from competitors or predators, but the necessary research has not been done. 

Based on an extensive review of available literature, my colleagues Marek Spinka, Ruth Newberry, and I proposed that that play functions as training for the unexpected by increasing the versatility of movements and the ability to recover from sudden shocks, such as the loss of balance and falling over, and to enhance the ability of animals to cope emotionally with unexpected stressful situations. To obtain this training, we suggested that animals actively seek and create unexpected situations in play and actively put themselves into disadvantageous positions and situations.

Comparative data from a wide range of species support this hypothesis. And, while it is difficult to test these ideas in the field, a study of mountain goat kids by Rachel Théoret-Gosselin, Sandra Hamel, and Steeve D. Côté called “The role of maternal behavior and offspring development in the survival of mountain goat kids“ showed that “play behaviors could enhance the emotional resilience to stress not only for unpredicted events but also in stressful group situations because play could reduce aggressiveness in gregarious species.” More field data are needed and this study is an excellent example of what needs to be done.

The play bow: Are dogs really confused when they play and what does this mean?

The authors also dismiss the detailed work that has been conducted on the play bow, a highly ritualized and stereotyped action by which animals signal their intention to play (please see accompanying image). When dogs and other animals bow they crouch on their forelimbs, raise their hind end, and occasionally wag their tail and bark. Coppinger and Feinstein write, “But we wonder if the so-called play bow in fact really has any adaptive, let alone cognitive, significance.” A good deal of very detailed research has been conducted on the bow by my research group and also by Barbara Smuts and her students that clearly supports the claim that bows are adaptive and have cognitive significance (please also see along with Mechtild Käufer’s excellent book called Canine Play Behavior: The Science of Dogs at Play and a comprehensive review essay by Elisabetta Palagi and eight other play experts called “Rough-and-tumble play as a window on animal communication“). The abstract for this excellent evidence-based and extremely significant up-to-date essay reads: Rough-and-tumble play (RT) is a widespread phenomenon in mammals. Since it involves competition, whereby one animal attempts to gain advantage over another, RT runs the risk of escalation to serious fighting. Competition is typically curtailed by some degree of cooperation and different signals help negotiate potential mishaps during RT. This review provides a framework for such signals, showing that they range along two dimensions: one from signals borrowed from other functional contexts to those that are unique to play, and the other from purely emotional expressions to highly cognitive (intentional) constructions. Some animal taxa have exaggerated the emotional and cognitive interplay aspects of play signals, yielding admixtures of communication that have led to complex forms of RT. This complexity has been further exaggerated in some lineages by the development of specific novel gestures that can be used to negotiate playful mood and entice reluctant partners. Play-derived gestures may provide new mechanisms by which more sophisticated communication forms can evolve. Therefore, RT and playful communication provide a window into the study of social cognition, emotional regulation and the evolution of communication systems.

The so-called play bow. Based on an unpublished student project in which “Border collies were confronted with normal and drugged roosters”,  Coppinger and Feinstein believe that the “so-called play bow” is a posture assumed by an animal confused by its next move. They write, “... the play bow occurs when an animal is in a temporarily indeterminate state ... In short, the ‘playing’ animal is in conflict about its next move - and the play bow in fact looks just like a combination of multiple conflicting behavioral shapes.” The authors ignore detailed research that shows how play bows are extremely stereotyped (they are what ethologists call a modal action pattern), they vary in shape and duration depending on where they are performed in a play bout, and they allow a dog to perform a wide variety of movements from this posture. There are no data that support their belief and the student’s data are impossible to assess. And, it’s not clear at all why they refer to the “so-called play bow,” when many researchers have studied it and concluded, based on substantial data, that it is indeed used almost exclusively in the context of play both as a play invitation signal and also to maintain the play mood. 

Let’s briefly think about what it means when a dog or other animal is confused, because every definition I can find indicates that there have to be cognitive and emotional underpinnings. In the case of dog-dog play, a simple view would be that Harry (a dog) wants to play with Mary (another dog) and that Harry isn’t sure what to do so he carefully pays attention to what Mary has done and is doing, and tries to factor this information into what she is likely to do in the future. In essence, Harry is pondering if he chooses to do “X” or “Y,” what will Mary do (and, of course, vice versa). Because play is indeed a hodge-podge of various actions, a kaleidoscopic behavior, on the authors’ view, Harry is confused, and to overcome his confusion he performs play bows.

There are no data that support the belief that dogs are confused when they play, however, there are data that show that there is a good deal of rapid of thinking and feeling on-the-run based on what Harry thinks and feels Mary is likely to do during the on-going interaction (and vice versa). These sorts of interactions make it clear that play is also a good place to observe and to study what researchers call a “theory of mind,“ because Harry and Mary need to pay very close attention to what each has done and is doing, and how that will influence what she or he is likely to do in the future (for further discussion please see Alexandra Horowitz’s essay called “Attention to attention in domestic dog (Canis familiaris) dyadic play“). There is a good deal of mind-reading going on here as Harry and Mary make careful and rapid assessments and predictions of what their play partner is likely to do. 

The cognitive and emotional underpinnings of “being confused” are rather rich, and do not lend themselves to simple mechanistic explanations that are favored by the authors. Available and ample data for a number of different species show there are predictable rules of play that cross species lines, namely, ask first, be honest, follow the rules, and admit you’re wrong. This is why play is so exciting to engage in and also so much fun to watch and to study. And, this is also why play among young and old dogs only rarely escalates into injurious aggression, although the authors recall an instance when play among four-week-old Border collie littermates was fatal and use this observation to claim that play “can itself cause significant harm” (p. 165). Indeed, Shyan, Fortune, and King (2003) reported that fewer than 0.5% of play fights in dogs developed into conflict, and only half of these were clearly aggressive encounters. Their data agree with our own observations on wild coyotes and free-running dogs at play.

Behavioral variability. Another example of a claim that is countered by available data centers on behavioral variability in young dogs and wolves. Coppinger and Feinstein write, “When we observe wolves, we see a similar picture. Wolf puppies are often noticeably more robust and varied in their play routines than dogs of the same size and age. This means, according to our hypothesis, that they should have more available motor patterns than the dogs do. That is in fact the case.“ (my emphasis) However, they offer no data. 

Along these lines, years ago Robert Fagen, another play expert and author of the classic book Animal Play Behavior, analyzed the sequential variability of play and aggression in young dogs (beagles), wolves, and coyotes using data my students and I collected, and discovered that social play in the beagles was more variable than social play in wolves and coyotes of the same age (and coyote play was more variable than wolf play). These data were published in an essay I wrote with John Byers (“A critical reanalysis of the ontogeny of mammalian social and locomotor play: An ethological hornet’s nest,” in K. Immelmann, G. W. Barlow, L. Petrinovich, and M. Main, Eds., Behavioral Development, The Bielefeld Interdisciplinary Project. New York: Cambridge University Press, pp. 296-337, 1981) that the authors list in their reference section. And, we also found that young beagles and wolves shared the same basic ethogram and number of motor patterns. Perhaps working dogs such as Border collies are different from beagles and other dogs, but we really don’t know if this is the case. 

The way in which the authors routinely dismiss a wealth of detailed research on animal play is characteristic of much of their book, that is essentially a tapestry of criticism using stories and unpublished projects in lieu of published data. It’s easy to see how one might walk away feeling that just about everyone else is wrong about dog behavior, cognition, emotions, and consciousness, and much of the research that has been done can be tossed into the garbage because it’s merely debris. 

All in all, the one-sided assault on the ever-growing literature in the growing field called cognitive ethology (the study of animal minds) fails. How Dogs Work does not really tell us how dogs work, but rather provides an extremely narrow view of mainly working dogs as machines. I find the topic to be of great interest and am always eager to learn more about why some people favor reductionist and mechanistic accounts to explain the behavior of complex sentient beings (see, for example, Sara Shettleworth’s book, Fundamentals of Comparative Cognition). However, How Dogs Work doesn’t convince me that the authors’ over-arching views are tenable. Beliefs don’t substitute for data that have been reviewed by peers, and there are plenty of data that are readily available. 

All in all, we really know far more than the authors offer, and for numerous wide-ranging and critical discussions of many different aspects of dog behavior I suggest  Domestic Dog Cognition and Behavior: The Scientific Study of Canis familiaris edited by Alexandra Horowitz, Adam Miklosi’s Dog Behaviour, Evolution, and Cognition, The Social Dog: Behavior and Cognition edited by Juliane Kaminski and Sarah Marshall-Pescini, and Mechtild Käufer’s Canine Play Behavior: The Science of Dogs at Play. For more on play I highly recommend the excellent and comprehensive review article by Elisabetta Palagi and her colleagues called “Rough-and-tumble play as a window on animal communication“ and (in addition to the references above) Sergio Pellis and Vivien Pellis’ The Playful Brain: Venturing to the Limits of Neuroscience.

What’s so incredibly exciting about the study of play behavior and the cognitive and emotional lives of dogs and other animals is how much we’re learning about how individuals negotiate challenging and complex social and non-social situations by carefully analyzing what’s happening and by using hard-wired actions when needed (for example, when they need to do the right thing instantaneously or the first time they are faced with a specific situation and there’s no room for error), along with behavior patterns that require careful thought and flexibility motivated by what individuals are feeling about the situation in which they find themselves.

Please stay tuned for more on dog behavior, cognition, and emotions, because there is a lot of research being done by research groups around the world, and we still have a lot to learn. Dogs are amazing sentient beings who challenge us in many different ways.

I thank a number of people for help with this essay.

Note: In a number of email messages I've been asked if I knew what happened to the 1000’s of sled dogs dogs for whom Dr. Coppinger was responsible. On page 25 we’re told, “Some four thousand dogs ‘went through the yard’” when “Ray spent fifteen years breeding and training dogs that pull sleds.” I have no idea what happened to these dogs, but according to some people I consulted, this is an incredibly large number of dogs, an average of around 267 a year. 

A century ago, pets didn’t even warrant the meager legal status of “property.” Now, they have more rights and protections than any wild animal on earth. How did we get here—and what happens next? That’s what Citizen Canine: Our Evolving Relationship with Cats and Dogs (Public Affairs) by David Grimm is all about.

Grimm discusses all aspects of the issue, providing readers with enough information so they can make their own decisions about whether humans should celebrate or condemn the better treatment of cats and dogs. We are entering a new age of pets/companion animals, one that is fundamentally transforming our relationship with them and reshaping the very fabric of society. Citizen Canine is an easy, enjoyable, must-read for all who want to know more about these fascinating beings.

(This post is a response to Which Emotions Do Dogs Actually Experience? by Stanley Coren, Ph.D., F.R.S.C.)

 

Dogs are amazing nonhuman animal beings (animals) and anyone who's known a dog knows this. Just today Dr. Stanley Coren published a very interesting essay called "Which Emotions Do Dogs Actually Experience?" and concluded, among other things:

"However, we know that the assortment of emotions available to the dog will not exceed that which is available to a human who is two to two-and-a-half years old. This means that a dog will have all of the basic emotions: joy, fear, anger, disgust and even love. However a dog will not have those more complex emotions like guilt, pride and shame." (After an email exchange with Dr. Coren about my response to his essay, he modified his conclusion to read, "However based on current research it seems likely that your dog will not have those more complex emotions like guilt, pride and shame.")

While this conclusion is extremely interesting, it remains a hypothesis in that the necessary research has not really been done. So, until the detailed research is conducted we don't really know "that the assortment of emotions available to the dog will not exceed that which is available to a human who is two to two-and-a-half years old."

We also don't know if dogs experience guilt, pride, and shame. However, because it's been claimed that other mammals with whom dogs share the same neural bases for emotions do experience guilt, pride, and shame and other complex emotions (see also and and), there's no reason why dogs cannot. And, there's solid biological/evolutionary reasons to assume dogs can and do. Recall Charles Darwin's ideas about evolutionary continuity in which the differences among species are seen to be variations in degree rather than kind - "If we have or experience something, 'they' (other animals) do too."

Do dogs feel guilt?

One more point needs to be made concerning doggy guilt. Consider the research conducted by Alexandra Horowitz, author of Inside of a Dog and Psychology Today writer. As I noted in a previous essay called "The Genius of Dogs and The Hidden Life of Wolves", Dr. Horowitz's research is often misinterpreted. For example, in their book titled The Genius of Dogs: How Dogs Are Smarter than You Think, Brian Hare and Vanessa Woods consider Dr. Horowitz's research on doggy guilt (pp. 183ff). They write that Horowitz "conducted an experiment to see whether dogs can feel guilty" but they misinterpreted just what Dr. Horowitz was actually trying to do. Her research did indeed show that people were not all that good at reading guilt in their dog, however her data do not show that dogs cannot feel guilt. I frequently hear people say that Dr. Horowitz's project showed dogs cannot feel guilt and this is not so (please see Dr. Horowitz's comment about this error).

Let's keep the door open about the emotional lives of dogs and other animals and also extend a hearty thanks to Dr. Coren for once again writing a very interesting and stimulating essay. 

Note: One can also question the value of comparing young humans with other animals. I don't find these comparisons to be especially compelling and other researchers have agreed that they are fraught with difficulties as are many cross-species comparisons concerning the cognitive and emotional capacities of individuals of different species. In a previous essay I wrote, "Animals do what they need to do to be card-carrying members of their species and we need to remember that numerous nonhuman animals outperform us in many different ways." Of course we are exceptional in various arenas as are other animals. Perhaps we should replace the notion of human exceptionalism with species or individual exceptionalism, a move that will force us to appreciate other animals for who they are, not who or what we want them to be.