Does this Smell Funny to You?

Are dogs self-aware? Do they recognize themselves as individuals, distinct from others?Other Animals Have It: Although rather tricky topics of study, animal self-recognition, self-awareness  and consciousness have been examined by scientists for decades. Animal consciousness is neither a new idea, nor is it a radical way of thinking. Lucky for us, we no longer live in the age of Descartes when animals other than those of the human variety were viewed as non-thinking automatons who lacked both consciousness and the ability to feel emotions. (Though, personally I can think of a few humans who may fit that description).

Evidence for at least a rudimentary sense of self-awareness is available in a wide range of non-human animal species. A leading theory of the evolutionary benefits of this trait is that the ability to distinguish self from other helps social animals (including humans) to recognize their place within their social group, to cooperate successfully with others, and to identify individuals who are outside of their  group. Dogs, also members  of a highly social species, are now known to have much more complex inner lives than we once gave them credit for. They readily follow the gaze of another dog or person, understand pointing, attend to the emotional states of others, and demonstrate rudimentary aspects of perspective taking (knowing what someone else can see or know). Having a sense of self as distinct from others is an additional cognitive talent that dogs may possess given their highly social nature and the functional benefits of self-recognition and self-awareness.

Mirror, Mirror: The classic test used to study self-recognition has been the mirror self-recognition (MSR) test. Using this method, the subject animal examines her image in a mirror after an area of her body has been surreptitiously marked with a spot of dye. The animal’s reaction to this alteration is observed and if  the subject uses the mirror to examine the spot on her body, this attention is interpreted as evidence for recognizing the image in the mirror as oneself rather than simply an image of a like-looking animal with a funny spot on her head.  Species that regularly pass the MSR test include the great apes (chimpanzees, bonobos, orangutans), dolphins, a single elephant, and even some bird species, such as the Magpie. Oh yeah, and most humans pass, as long as they are older than 2-years of age.

MAGPIES PASS IT

What about Dogs? Dogs however, have routinely failed this test. Dog folks are now certainly muttering, “Well of course, dogs do not use vision as their primary special sense – they use olfaction – their noses“. This difference is significant, since dogs believe what their nose tells them first and foremost, compared with primate species such as ourselves, who perceive the world primarily through vision. Additionally, because of anatomical and social differences, dogs do not regularly self-groom in the same manner that primates do, so are not as apt to care about an unexpected spot that suddenly shows up on the top of their head. For those who study dogs, clearly, another type of test was needed.

Enter Alexandra Horowitz and her team of dog pee researchers at Barnard College in New York City.

The Significance of Pee: Dogs regularly investigate the urine scent of other dogs. There is evidence that they spend more time investigating the urine markings of other dogs and less time sniffing their own urine, which suggests that dogs distinguish their own scent from that of others. Using this knowledge, Horowitz devised a new type of mirror test for dogs – this one based upon their primary sense – smell. She reasoned that just as a chimpanzee notices the sudden change in appearance when a spot of dye shows up on her head, if dogs recognize their own scent, then they too should be surprised to find an unexpected change in that smell and attend to it (sniff it) for a longer period of time. She devised a pair of controlled experiments that asked, using their sense of smell –  “Do dogs recognize themselves?”

The Study First, the team of researchers collected the pee of a group of volunteer dogs (well, okay, the owners volunteered their dogs’ pee. We are not really sure how the dogs felt about that part). The author also collected urine from her own dog, who would serve as the “unfamiliar dog” sample. Each dog was tested individually with a set of three scent canisters for three separate trials and comparisons. One canister contained water only (decoy sample),  one contained the subject dog’s urine (self), and the third contained either (1) the subject dog’s adulterated urine (marker self), (2) the urine of an unfamiliar dog (other), or (3) the scent of the adulteration substance alone (marker). Two experiments were conducted, with the only difference being the way in which the subject dog’s urine was altered. In Exp. 1, a tissue sample of dog spleen was added to the urine. In Exp. 2, a small amount of anise essential oil was added.

Results: Similar to mirror tests, the researchers expected dogs to pay more attention to a scent of themselves that was unexpectedly altered compared with their reaction to their unaltered urine scent. Here is what they found:

  1. Who’s this guy? As earlier research has shown, dogs spent more time investigating the urine of an unfamiliar dog compared with the time that they spent sniffing their own urine. (“Hmm…. Smells like I was here earlier……whoa…..hello….who is this new dude who peed here too?)
  2. Hey Sally! Interestingly, dogs did not spend more time investigating the urine of a known dog (their housemate) compared with time spent smelling their own urine. (Looks like Sally was visiting at the same time I was. Funny, I don’t remember seeing her here….”)
  3. Does this smell funny to you? Last, dogs spend significantly more time investigating the canisters that contained their altered urine scent compared with how long they investigated their unadulterated urine. This difference occurred with both types of marker substance – spleen tissue and anise oil. Dogs also returned to the canisters more often when their urine was compared with their adulterated urine.  (“Wowza. This is weird. Did I eat something odd last night? Maybe I am getting a cold? What the heck IS that smell on me???”)

The authors conclude that these results support the use of their newly designed (and quite ingenious, if I may add) “smell test” as species-relevant analog to the MSR test. The fact that the dogs spent more time investigating their own urine when it had been unexpectedly changed supports some level of recognition of their own odor and by extension, perhaps a rudimentary “sense of self”. Similarly, dogs were highly interested in the scent of unfamiliar dogs (Hey! Who’s this guy??) but not to the odor of their housemate.

Yeah, I have an opinion on this one. First though, I have to say that this is one of the most creative and clever studies that I have read in some time. (Not to mention it being ripe for witticisms and puns……).

The results of this study suggest that dogs may possess one of the cognitive traits, self-recognition, that humans have historically co-opted for our species and our species alone. In past, we have worked diligently to make clear cognitive distinctions between human animals (us) and non-human animals (everyone else). A wide range of traits have been used for this purpose, many of which have fallen like a house of cards as they are discovered to exist in other animals. Examples include the expression of emotions, perspective taking, tool use and tool making, existence of culture, ability to reason, and the demonstration of altruism. We also know that humans do not hold exclusive rights to the expression of self-awareness and consciousness and are not the only species capable of complex thought, internal representations of the world, planning, intention and deception. Yeah, we do have language and we are capable of “meta-thinking” (thinking about thinking), but many types of cognition and complex thought have been demonstrated to exist in some form in a host of other animals, including dogs. So what is the big deal? Is there really anything to argue about here? Well, yeah, as a dog trainer (a clicker trainer, I must emphasize), I think that there is an important point to be made.

It is this. Behaviorism alone can no longer be enough. The science of behaviorism and its application in dog training no longer can adequately capture and address all that is dog. Sorry to all of you purists out there, but there it is. (And remember, I am a clicker trainer).

Here is my argument: Although dogs respond well to the laws of behaviorism (just as humans do), the fact that we successfully use operant and classical conditioning to train dogs should not be confused for evidence that dogs are lacking in a host of mental skills that fall higher on the cognitive complexity scale. Behaviorism and social cognition are not mutually exclusive sciences (though to listen to some trainers and some scientists, you would think they were disciplines existing on different planets).

The reason that I bring up this particular issue in this particular essay is because self-recognition and self-awareness seem to be a current “hot spot” in this debate between behaviorism and cognitive science. Pure behaviorism has its benefits – mainly it works great when applied as a training technique. However, given the boatloads of research published by cognitive scientists that demonstrate the social complexity of the domestic dog (and now – self-recognition!), we cannot discount as trainers evidence showing that dogs pay attention to the social cues of humans and of other dogs, that they possess some level of perspective taking, that they regularly learn through observation of others, that they can recognize one another and understand intent by the sound of their barks, and that they can recognize one another and themselves through smell. It is time for trainers to embrace both of these important and enlightening bodies of science. We should support and use behaviorism because it provides simple and elegant rules for training that work, and we must also encourage studies of canine social cognition because they continue to teach us more about the internal lives, experiences and perceptions of our canine best friends.

Off of soap box. Back to pee jokes.

Cited Study: Horowitz, A. Smelling themselves: Dogs investigate their own odours longer when modified in an “olfactory mirror” test. Behavioural Processes, 2017; In Press.

Fear Itself

Last year, on the drive home from our annual vacation in Bar Harbor, Maine, our 11-year-old Brittany, Vinny suddenly and inexplicable awoke from a sound sleep and began to tremble, pant, pace, and obsessively lick at the sides of his travel crate. When I crawled back over the seat to find out what was wrong, Vinny’s eyes were “squinty” and he avoided looking at me as he continued to lick and pant. Mike immediately pulled over to a rest area and we got Vinny out of the car. As soon as he was on the ground and moving about, Vinny relaxed, looked at us calmly, gave each of us a nice Brittany hug, and off we went for a little walk. Perplexed, we thought that maybe he had to eliminate (nope, no urgency there), was feeling carsick (no signs), or had a bad dream (who knows?). Within less than a minute, our boy was his typical happy self, showing no signs at all of distress. We loaded all of the dogs back into the car and Vinny continued the journey home with no further incident. We still are not sure what triggered this odd stress episode in our boy. He has had one (equally perplexing) recurrence since, continues to be healthy and happy, and we continue to monitor him carefully both at home and when he is traveling with us.

Vinny Loves Bar Harbor

HAPPY VINNY IN BAR HARBOR, MAINE

Recognizing Stress and Fear

It is important for dog owners to recognize and respond to signs of stress and fear in our dogs. If we are sensitive to their emotional states and are accurate in our interpretations, we can respond appropriately to situations in which a dog is uncomfortable, stressed, or frightened. Because nonspecific signs of stress can be the first signs of illness or injury, attending to these promptly may help us to get our dogs the medical attention that they need before conditions worsen or escalate into an emergency. It is well-known that perceiving and understanding the emotions of others is a basic human social skill. We use these perceptions on a daily basis when we interact with other people – family members, friends, and even strangers. Interestingly, while most of us are capable on some level of reading the emotional states of other humans, studies have shown that these abilities vary tremendously among individuals. Similarly, because many share our lives with dogs, it follows that we use these same skills when interpreting the emotions of our canine friends.

fearfuldog15

CAN YOU RECOGNIZE FEAR IN DOGS?

Studying Perceptions

However, until recently, the accuracy of our perceptions of dogs’ emotional states had not been studied. Two research studies examined the cues that we use and our levels of accuracy when we perceive fear and stress in our canine companions.

Study 1: The first was conducted by researchers in the Department of Psychology at Columbia University in New York (1). The study team produced a series of video clips of dogs and embedded them in an on-line survey. Participants viewed the videos and then were asked to classify each dog’s emotional state using one of five possible descriptors (angry, fearful, happy, sad, or neutral). The first four of these are called “primary emotions” and were selected because research has supported the existence of these emotions in dogs and other animals. Although the study participants had 5 choices, the videos in the study only showed dogs demonstrating two possible emotions, either happiness or fear. All of the videos had been pre-categorized into the two emotion categories by a panel of dog behavior experts prior to the start of the study. After identifying each dog’s emotion, participants were asked to describe the specific features of the dog that they felt led them to their conclusion. For example, if a person classified a dog as showing happiness, she might say that the dog’s facial expression, ear set, and wagging tail were important features that conveyed this state to her. Last, the participants were asked to rate the level of difficulty that they experienced while attempting to interpret the emotions of each dog and to provide an estimate of overall confidence in their accuracy.

Results: Over 2000 people completed the survey and were divided into four dog experience categories based upon their dog ownership and professional histories. These were non-owners, owners, dog professionals with less than 10 years of experience, and professionals with more than 10 years of experience. It was somewhat surprising to find that the vast majority of people who completed the survey, more than 90 percent, correctly identified happy dogs in the video clips, regardless of the person’s level of dog experience. This means that most people, even those who have never owned a dog, could look at a happy dog and see…..a happy dog! This is good news.

Happy Face 3

PEOPLE KNOW A HAPPY DOG WHEN THEY SEE ONE!

However, when it came to recognizing fear in dogs, the news was not quite so positive. While more than 70 percent of dog professionals correctly identified the fearful dogs, this proportion dropped to 60 percent of dog owners, and to only 35 percent of non-owners. Put another way, this means that 40 percent of dog owners and 65 percent of non-owners were unable to correctly identify signs of fear and stress in an unfamiliar dog. Moreover, a substantial number of the non-owners (17 percent, or about one in six people) misclassified a fearful dog as a happy dog. This statistic is especially troubling, given the potential dangerous outcome of such mistakes. A person who approaches a dog who they believe to be friendly but who in effect is fearful, will at the very least increase the dog’s fear and distress and could potentially cause a defensive response in the dog, leading to a snap or bite. The features of the dogs that participants used to make their decisions also varied with experience level. A person’s tendency to focus on a dog’s facial features (eyes, mouth, ears) increased significantly along with experience. Inexperienced participants used primarily the dog’s tail and body posture to inform them about the dog’s emotional state. Conversely, more experienced people identified both facial expressions and body postures as important features when assessing a dog.

Interestingly, but perhaps not surprisingly, the results of this study are consistent with studies of human abilities to perceive and interpret the expression of emotions in other people. We are generally more sensitive to and more accurate at interpreting happy facial expressions in other people than we are when responding to fearful expressions. Moreover, while social experience seems to have little effect upon our responses to happy faces (we show a proficiency to do this at a very young age), having varied and extensive social experience is an important factor in determining our success at perceiving fear and stress in other people. In dogs, this study tells us that dog-related training and experience enhance our tendency to pay attention to dogs’ facial expressions along with their body postures and enhances our ability to correctly perceive fear.

Study 2: While the first study provided a general test of how people perceive fear in unfamiliar dogs, the second examined the ability of dog owners to recognize signs of stress in their own dogs (2). This study was conducted by researchers at the University of Pisa in Italy with a group of almost 1200 dog owners recruited through veterinary clinics. Participants first completed a questionnaire in which they were asked about stress in dogs and its potential health and behavioral consequences. They then identified what they believed to be signs of stress in dogs and estimated the level of stress in their own dog.

Results: More than half of the owners (60 %) were found to have a clear understanding of what stress is and how it can affect a dog’s emotional state and health. However, about 20 percent of owners (one in five) believed that experiencing stress had no negative physical or emotional consequences on dogs. (In other words, while they agreed that it occurred, they thought it was no big deal). The behaviors that owners most frequently identified as reflecting stress in their dog included trembling, whining/crying, excessive barking, and panting. In contrast, very few owners identified more subtle behaviors such as avoiding eye contact, turning away, yawning, nose licking, or yawning as signs of stress in dogs. Those owners who self-reported as being highly concerned with their dog’s stress level were more likely to identify these less obvious signs as important. Overall though, owners tended to miss many of the facial expressions (squinty eyes, avoiding eye contact, changes to ear set, retracted commissures) that most trainers immediately look for when they are assessing a dog’s stress level. Like the first study, this suggests that it is these more subtle facial cues of stress and fear that may be missed if a person is only paying attention to the more obvious body posture signs.

Take Away for Dog Folks

These two studies provide complementary information about the behavior cues that people pay attention to when attempting to decipher a dog’s emotional state. The first showed that even inexperienced people were able to correctly identify a dog who is happy and relaxed. However, perceptions of fear were strongly correlated to how much prior experience a person has had with dogs. As experience level increased, not only were people more likely to be correct, but they also were more likely to pay attention to a dog’s facial expressions than were people who did not spend much time with dogs. We also learned that dog owners are more likely to focus attention on their dog’s body posture, vocalizations and movements than on the more subtle signs of stress that involve a dog’s facial expressions and eyes.

Why it matters: Accurately recognizing fear and stress in dogs is an important skill set to have. Understanding our own dog’s emotional state allows us to respond by helping him out of situations that cause fear and reducing or eliminating triggers of stress when they are under our control. For trainers and behaviorists, working with owners who are sensitive to their dog’s stress response promotes the development of a more effective training and management plan. On a societal level we all benefit from a universal understanding of the behaviors, body postures and facial expressions that convey happiness versus fear or stress in dogs. Correctly interpreting a dog’s behavior is always enhanced by attending to both body posture and facial expressions. However, interpretation of dogs’ facial expressions may not come naturally to many people. This knowledge emphasizes the importance of teaching the subtleties of canine facial expressions in training classes, behavior education courses, and bite prevention programs. Moreover, the statistic suggesting that one in five owners do not consider the effects of stress in their dogs to be of negative consequence tells us that education is also needed regarding the health and welfare impacts of stress and fear on our dogs’ well-being and quality of life.

Here at home, Mike and I are still uncertain about what caused Vinny’s acute stress response during our vacation trip. As Vinny has aged he has become somewhat more sound sensitive, which is not unusual in senior dogs. However, even though we responded quickly at the time and he apparently recovered, we did not learn enough from the episode to determine a possible underlying cause. Perhaps we will never know. Regardless, I do know that paying attention to all of Vinny’s signs – body language, facial expressions, and eyes, will help me to understand him, care for him, and love him as best we can.

Vinny and Cooper Aunt Betty Pond Run

SENIOR BOY VINNY HIKING WITH HIS PAL COOPER IN BAR HARBOR

Cited References

  1. Wan M, Bolger N, Champagne FA. (2012) Human perception of fear in dogs varies according to experience with dogs. PLoS ONE 7(12): e51775. doi: 10.1371/journal.pone.0051775
  2. Mariti C, Gazzano A, Moore JL, Baragli P, Chelli L, Sighieri C. (2012) Perception of dogs’ stress by their owners. Journal of Veterinary Behavior 7:213-219.

NOTE: A version of this article was published in the December 2014 issue of Whole Dog Journal and is also included in my newest book, Beware the Straw Man: The Science Dog Explores Dog Training Fact & Fiction“.

 

Fear Factor

Experiencing fear is not pleasant. Any human will tell you this. As one of our most basic emotions, fear functions as a rapid-fire means of communicating to our bodies  “DANGER, DANGER – GET AWAY NOW!!”

Running from Tella Tubbies

OF COURSE, WE ALL TEND TO FEAR DIFFERENT THINGS….

As a physiological state, fear is associated with a set of bodily changes that are decidedly uncomfortable.  Respiration and pulse increase, we become hyper-vigilant of our surroundings, our hearts pound, and we may experience a strong inclination to flee (especially considering that Tella Tubbies run really fast despite their portly dimensions).

Dogs who experience fear exhibit the same physiological signs as humans and most likely also suffer the same unpleasant emotional state. Common fears/anxieties in dogs include separation anxiety, fear of unfamiliar people or dogs, and sensitivity to  thunder or loud noises. When these problems persist over long periods of time, they will definitely reduce a dog’s quality of life and can negatively affect the relationship between the dog and his or her owner. In addition, long-term exposure to stress may affect dogs’ physical health and longevity.

Background: There  is evidence in humans and in laboratory species that experiencing prolonged periods of stress and anxiety  increase an individual’s susceptibility to disease and risk of premature death (1-3). A possible underlying cause for this effect may be chronic activation of the hypothalamic-pituitary-adrenal [HPA] axis, which is part of the body’s natural defense against physical and psychological stressors. It is the HPA system that is responsible for elevated levels of cortisol, that well-known hormone that prepares one’s body for flight or fight. Although cortisol is highly effective in the short-term, prolonged exposure to high circulating levels is associated with a number of chronic health problems, such as hypertension, insulin resistance, heart problems and immune disturbances.  Increased oxidative  stress also occurs during exposure to physical or emotional stressors, and is associated with an increased rate of cellular aging and death. Although the exact underlying mechanisms are not fully understood, it is well-established that living in fear is not good for us.

funny-fear-duck-watching-you

WHATEVER YOUR FEAR……ITS NOT HEALTHY.

What about dogs? Although the relationship between prolonged stress, health and lifespan is an active area of research in human subjects, until recently this association had not been studied in dogs.

The Study: Nancy Dreschel, a veterinarian at Pennsylvania State University, asked the question: “Are dogs who are more anxious or fearful at increased risk for health problems and a shortened life span?”(4).  The study used a web-based questionnaire to collect information from people who owned a dog that had died within the previous five-year period. The survey included questions about the dog’s demographics, social environment, behavior, training history, health, and daily interactions with the owner. A set of questions adapted from the validated C-BARQ program  was used to collect detailed information about the presence or absence of fear-related and anxious behaviors. Age and cause of death were also recorded. The survey was available on-line for 7 months and resulted in 721 complete surveys that were used in the analysis.

The Results: As expected, body size and weight were negatively correlated with lifespan. It is well-established that large/giant dogs have a shorter average life span than small and medium size dogs. In addition, neutered dogs had a longer lifespan than intact dogs and accidental deaths were associated with a younger age of death. When body size, neuter status, and accidental death were controlled for, several significant relationships were found between behavior and lifespan:

  1. A significant negative correlation was found between the fear of unfamiliar people and lifespan. This means that dogs who experienced a lifelong fear of strangers tended to die at a younger age than dogs who did not experience this type of fear.  However, the earlier age of death in this subset of fearful dogs was not associated with any particular disease. (Because long-term activation of the HPA axis negatively affects the immune system, it was speculated that fearful dogs would be more susceptible to cancer, infections, or immune-mediated disorders. However, this relationship was not found in these data).
  2. The presence of non-social fears (fear of new places or things) and separation anxiety were both positively associated with chronic skin problems. The underlying mechanism might be the effects of long-term stress on the immune system and skin health, a relationship that has been reported in human subjects. However, this study’s design did not allow determination of causation, so conclusions regarding the underlying cause for this relationship could not be made.
  3. Lifespan was strongly and positively correlated with owner-reported “good” behavior. Dogs who were perceived as being well-behaved by their owner lived longer than those who were reported to be less well-behaved. Multiple factors may have been in play with this relationship. Because problem aggression was not specifically studied, euthanasia for aggression may have been a significant contributing factor. Less dramatically, owners who reported their dogs as less well-behaved may have been less bonded to the dog and more likely to euthanize at a younger age or to decline treatment for a serious illness. It is also possible that well-behaved dogs tend to live longer because they experience a less stressful and more harmonious home environment with their owner. Because none of these factors were studied separately, the exact cause or causes of this relationship could not be teased out, but certainly warrants additional study.
Feraful Dog Greeting

Chronic Fear of Strangers is Related to Decreased Life Span

Take Away for Dog Folks: Remember that survey studies provide information through the eyes of the owner and, in this case, the collected data were also retrospective (historical) in nature.  These factors must always be considered when making conclusions about survey studies. In addition, the statistical tests used in this study tell us if two or more factors are related (i.e. correlated), but cannot provide information about the direction of that relationship or if there is another underlying cause that was not identified.  Even considering these limitations, the results of this study suggest that prolonged fear and anxiety not only impact a dog’s quality of life, but may also contribute to an early death and increased susceptibility to chronic health (skin) problems. Helping dogs to overcome fear is vital to improving their lives and our relationships with them. For those of you who are working with these dogs on a daily basis, thank you for all that you do (5).

References and Information Sources:

  1.  Cavigelli SA, McClintock MK. Fear of novelty in infant rats predicts adult corticosteroid dynamics and an early death. Proceedings of the National Academy of Science USA 2003;100:16131-16136.
  2. McEwen BS. Stressed or stressed out? Journal of Psychiatric Neuroscience 2005; 30:315-318.
  3. Schultz R, Beach SR. Caregiving as a risk factor for mortality. Journal of the American Medical Association 1999; 282:2215-2219.
  4. Dreschel NA. The effects of fear and anxiety on health and lifespan in pet dogs. Applied Animal Behaviour Science 2010; 125:157-162.
  5. An excellent source of information for working with fearful dogs is Debbie Jacob’s book “Guide to Living With & Training a Fearful Dog and her blog, Fearful Dogs.