If They Can't See Me, They Still Might Hear Me: Dogs Think About Sound When Stealing Treats (or Chasing Suspects?)

Canine sensitivity to human social and communicative cues has been the subject of significant research in a number of labs for several decades. Research has also looked at whether dogs are concerned with our attentional states, e.g., whether their behavior changes when we’re looking at them. If a dog is told not to eat a piece of food on the floor, the dog is more likely to obey if the human giving the command is watching the dog (and more likely to disobey if he is not watching). Even if the dog cannot resist the temptation to get to the food when the human is watching, it will do so in a more indirect manner, such as by trying to sneak up from the direction the human is not looking. I reviewed a number of studies to this effect in Service and Therapy Dogs in American Society (section on Eye Contact, beginning at page 22).

Recently, a research team designed an experiment to consider whether a dog’s behavior in taking a piece of forbidden food would differ when the dog could take the food silently from situations where taking the food would require making noise. They found, not surprisingly, that the dogs preferred to take the food in a way that didn’t make noise. The researchers tested dogs living in private homes as well as dogs from a shelter, the idea being to determine whether living with an individual or a family would affect a dog’s ability to use auditory information. There were 22 privately owned dogs used in the study, and 24 shelter dogs.

Food used for the study consisted of hot dog segments, bacon strips, and commercial dog treats. Food was placed in containers. All containers had brass bells hung across the opening, but for half the containers, the ringers had been removed. Owners of private dogs were asked what commands they would use to tell a dog to leave food alone. Dogs from shelters were told, “No.” Trials were videotaped. A dog was put about 1.5 meters from two containers, one of which was silent and one of which was noisy. The experimenter stood between the containers. The dog was held on a leash by someone else. After getting a dog’s attention, the experimenter put a treat inside each container. The experimenter demonstrated the auditory properties of the container by moving the string holding the bells five times. The noisy container rang during this manipulation, while the silent container did not. The dog was told “No,” or “Wait,” or another command designed to discourage it from going to the treat. The experimenter then adopted a Looking or Not Looking position. In the Looking position, she sat between the containers and looked straight ahead. In the Not Looking position, she put her head between her knees and faced the ground. The dog was then released from the leash. Everything was a double blind as possible.

The results indicated that dogs significantly preferred the silent container only in the Not Looking situation. When the experimenter was looking, there appeared no need for silence and they would almost as often approach either container. No significant difference was found between the privately owned dogs and the shelter dogs, so it does not appear that socialization in a family is essential to a dog’s capacity to consider the effect of sound. The authors note that these results could have significance in law enforcement and military contexts. Although they do not speculate further on this suggestion, it is possible to imagine that training a dog in suspect apprehension could be designed to take into account how a dog’s ability to surprise and subdue a suspect will be increased if the dog is sensitive to the suspect’s ability to hear its approach.

Kundey, S.M.A., De Los Reyes, A., Taglang, C., Allen, R., Molina, S., Royer, E., and German, R. (2010) Domesticated Dogs (Canis familiaris) React to What Others Can and Cannot Hear. Applied Animal Behaviour Science, 126, 45-50.

A question that might be worth investigating is whether different breeds show specific patterns to making sounds. A study by researchers in Hungary looked at reactions of dogs selected from three breed groups (Belgian shepherds (Tervuerens and Groenendaels), retrievers (golden and Labrador), and sled dogs (malamutes and huskies)). The sled dog group and the retrievers continued to show friendly, tolerant behavior even when a stranger approached in a threatening manner, but half the Belgian shepherds responded to threatening behavior with their own aggressive and threatening behavior. Even those shepherds that did not respond aggressively did not ignore the threatening behavior. Thus, a threatening suspect might elicit different levels of responses from different breeds of police dogs. Sound factors might be worth investigating in such contexts. Vas, J., Topal, J., Gacsi, M., Miklosi, A., and Csanyi, V. (2005). A Friend or an Enemy? Dogs' reaction to an Unfamiliar Person Showing Behavioural Cues of Threat and Friendliness at Different Times. Applied Animal Behaviour Science, 94, 99-115.

Dogs Misled by Strangers as Well as Owners in Food Choice Experiment. Another recent piece of research considered whether dogs, in a food choice experiment, were misled more easily by their owners than by unfamiliar but friendly humans. Thus, if dogs could choose between a slice of dry sausage and a (presumably) unappetizing pellet, would the pointing of the handler towards the pellet be more persuasive than the pointing of a stranger, despite the dog having seen where the tastier item was placed. The researchers found that dogs were misled almost as much by strangers as by their handlers. Marshall-Pescini, S., Prato-Previde, E., and Valsecchi, P. (2010) Are Dogs (Canis familiaris) Misled More by Their Owners than by Strangers in a Food Choice Task? Animal Cognition (not yet in print). As I’ve said before, they trust us too much.

Studies on Other Species. These types of two-choice tests have been done with other animals besides dogs, including chimpanzees and macaques. The picture shows a wolf in a two-choice test with a human pointing towards one of the choices. Here, researchers found that wolves could be trained to react to human pointing gestures, an ability that may have been significant during the process of domestication. Viranyi, Z, Gacsi, M,, Kubinyi, E., Topal, J., Belenyi, B., Ujfalussy, D., and Miklosi, A. (2008). Comprehension of Human Pointing Gestures in Young Human-Reared Wolves (Canis lupus) and Dogs (Canis familiaris). Animal Cognition, 11, 373-387.

Dogs Distinguish Types of Warning Growls

Animals have been shown to make sounds that are context specific, such as alerting other members of the group to a predator, even a specific type of predator. Dogs, like wolves, bark, but dogs bark more frequently and in more variable contexts than is the case with wolves. Both dogs and wolves growl in three situations that were studied in a recent paper: (1) offensive threatening in social conflict, (2) guarding food, and (3) during social play. Calls are described as functionally referential if three criteria are satisfied:

1. The signals displayed in different contexts have different acoustic structures.
2. Prerecorded signals evoke different behavioral responses in a playback experiment.
3. The manipulation of the referent alters the signal production.

A group of Hungarian and Austrian scientists recorded growls during three situations: (1) a dog guarding his food from a strange dog (a food-guarding growl, FG); (2) a strange human approaches a dog threateningly (threatening growl, TS); and (3) the dog plays tug-of-war with his owner (play growl, PL). The play growls were less than half as long as the two other types of growls. In a playback experiment, the researchers looked to see whether a food-guarding growl would cause another dog to retreat despite the physical absence of the dog making the sound. The threatening growl was also used in the same context to see if it would have an equally strong deterrent effect. The expressions of the dogs were different in the contexts of the growls. Thus, dogs growled at a threatening human with a closed mouth, but while defending food against another dog, they showed their teeth and pulled back their lips.

In the experiment, an owner and dog entered a room with a bone, which the dog was allowed to sniff but not touch. After a knocking signal from the experimenter, the owner released the dog. The owner was told not to talk, touch, or look at his dog. If the dog got within 5 cm of the bone, a pre-recorded growl was played. If the dog withdrew, the growl recording stopped paying. If the dog approached the bone again, the growl was played again.

The results were dramatic. After hearing the growl for the first time, 11 of 12 dogs in the FG group withdrew from the bone within 15 seconds, whereas only 2 of 12 dogs in the TS group and 4 of 12 dogs in the PL group withdrew in that period. Seven dogs in the FG group did not approach the bone again within the next 90 seconds, while only one dog in the TS group and one in the PL group stayed away. It was clear that FG growls had a stronger deterrent effect than TS growls though both were in the “agonistic” category of sounds. The researchers also found that the growls of bigger dogs had no measurably greater deterrent effect than the growls made by small dogs, confirming at least in part the common belief that dogs don’t think much about size. Farago, T., Pongracz, P., Range, F., Viranyi, Z, and Miklosi, A., ‘The Bone is Mine’: Affective and Referential Aspects of Dog Growls, Animal Behaviour vol. 79, 917-925 (2010).

Are Breeding Programs Reducing Genetic Variability?

There are various conflicts in the dog world. Choke vs. no-choke in dog training. Treats vs. other rewards. One that I’ve encountered more in the last few years are disputes between those who want to keep breeds pure vs. those who believe in crossing in other breeds. Some remarks near the end of Adam Miklosi’s wonderful book, Dog Behavior, Evolution, and Cognition (Oxford University Press 2007) are worth considering:

"Today dogs are subject to a dangerous ‘game’ which involves irresponsible playing with one tiny aspect of their phenotype: the form. This leads to two important problems. Breeders are encouraged to inbreed in order to fulfil the requirements which lead to genetically homozygous populations, and the absence of selection for behaviour leads to the disappearance of breed-specific traits. Thus this trend brings nothing good for dogs in terms of their evolution because genotypes are being lost and genetic variability is decreasing."

Miklosi then cites P.D. McGreevy and F.W. Nicholas, whose article, “Some Practical Solutions to Welfare Problems in Dog Breeding,” 8 Animal Welfare 329-341 (1999), argued that breeds should not be considered closed populations, and dogs from other breeds should be crossed in. This would not change the appearance of the breeds, as breeding programs can create virtual breeds, as was done with the Pharaoh Hound (described by Miklosi, in another section of his book, as “probably a fake ‘look-alike’ recently created from different types of dogs”).

My father, M.E. Ensminger, would have agreed with the notion of breeding in animals from other breeds. In his treatises on Animal Science, Beef Cattle Science, and other books, he placed a high value on “hybrid vigor,” recommending that breeding programs regularly cross in other breeds to improve production. He had the advantage of working with the livestock production field where appearance is important, but other qualities, such as the amount of muscle that becomes hamburger, were even more important. Consequently, I'm not aware that he encountered much resistance to his arguments. (His books are still in print, being revised under a trust arrangement by staff at Iowa State University.)

Those concerned with dogs losing behavioral characteristics as a result of crossing in other breeds should consider the research of Kenth Svartberg, a Swedish scientist, who studied breed differences using tests of over 13,000 dogs in 31 breeds. Svartberg concluded that selection was often being dominated by show dog breeders, and that their programs were producing good show dogs, but that the behaviors correlated with the breed origins, often inconsistent with what is required for a show dog, were disappearing. Kenth Svartberg, “Breed-Typical Behaviour in Dogs—Historical Remnants of Recent Constructs?” 96 Applied Animal Behaviour Science 293-313 (2006).

My aunt, Lee Watts, was a well-known poodle breeder in Canada. She used to say that if you didn't get a purebred dog, "you don't know what you're getting." I still hear it when I go to obedience classes. What she didn't know, and what Svartberg's research indicates, that you may be getting the right form, but as time goes on you're not getting the same complex of behaviors. Domestication does not stay still for other factors, even if the form stays still.

Additional Note.  The effect of letting show appearance dominate the breeding programs of a particular dog was decried long ago. Captian von Stephanitz, discussing the Scotch shepherd dog or collie in The German Shepherd Dog in Word and Picture (1923), noted that it is divided into "two varieties, a short smooth haired, and a long smooth haired kind, from which originated the long haired dogs so prized by the fancy breeders…. In the Shetland Islands, where the dwarf horse is bred, there is a dwarf variety of this collie.”  He then says a picture of a long haired dog that was “a prize winner of some reputation, shows how far one-sided and exaggerated breeding may go till it becomes unnatural and a caricature.  The collie of the fancy dog breeder is now only bred for beauty and is kept for luxury and show; with his slender small head and overbred face drawn out into an overlong nose—(this part from the tip of the nose to the division in the forehead is much longer than the cranium, while the proportion should be the reverse). Then there is the carriage of the ears, where only the upper third of them should tip over; but must only droop over that much, otherwise it is considered a great fault—(to the fancy breeder the erect eared Scotch dogs such as are also seen today are villainous rogues, worthy of death), and in conclusion the hair is everything…. The daily ‘toilet’—here the word must be understood in the English sense—of a collie beauty takes hours to perform; especially before an Exhibition.”

After discussing the show preparations that he finds offensive, Stephanitz then delves into the uselessness of the dog for real work:

“He lives more on the good reputation built up by the yeoman services of his ancestors, which he no longer knows how to perform. That is the meaning of the vacuous appearance of the shallow, unintelligent, ant-eater-like too elongated head…. The present day fancy Scotch dog with his slender needle like sharp teeth can tear very savagely and make serious wounds, but these qualities do not fit him for service with flocks and hers; and further, he lacks the strength necessary to stop and turn a stubborn sheep.”

Why Do Dogs Respond to Our Social Cues?

A focus of research on dog behavior has concerned the ability of dogs to respond to our social cues. In object choice tasks, a dog will have to decide which of two or more containers contains food. With certain controls, the dog unaided by a human will only perform at chance levels. If, however, a human points to the correct container, the dogs will much more likely go to it than the others. Even a human moving his eyes from the dog to the correct container and back and forth in this manner will help the dogs make the right choice, though not as often as pointing. Dogs will also choose the container a human is pointing at even if this is the wrong container, they’ve had a chance to smell the container with the food, and their noses should tell them to ignore the human’s pointing gesture. They trust us even when they shouldn’t. These findings, long known among canine behaviorists, lead to another question. Why do they follow our gestures when other animals, such as apes, don’t? Do they know we are trying to help them? Have they learned to trust us in the process of domestication? Pamela J. Reid of the ASPCA’s Animal Behavior Center in Urbana, Illinois, recently reviewed the literature on this topic, looking at the various hypotheses that have been propounded to explain why dogs read us so well. She distilled the conclusions of prior researchers down to four basic theories:

1. Dogs learn to respond to human social cues through basic conditioning processes.
2. Dogs reduced their fear of humans in the process of domestication and began to apply all-purpose problem-solving skills to their interactions with people.
3. Dogs’ co-evolution with humans equipped them with the cognitive machinery to respond to human social cues and understand our mental states (sometimes called a “theory of mind”).
4. Dogs are adaptively predisposed to learn about human communication gestures.

Reid herself favors the fourth explanation.

As to the first of the four theories, Reid notes that although dogs respond better to social cues after training, they perform significantly above chance even without prior experience with a pointing cue. Wolves raised the same way as dogs will not succeed as well as dogs in responding to pointing gestures.

Some researchers have argued that selection pressures placed on dogs for tameness and other desirable traits may have also been a stimulus for dogs to develop a specialized set of social skills. Dogs have learned to eat in the presence of humans and to accept restraint and in the process of domestication became expert readers of human social cues. Most (but not all) studies have found that dogs respond to social cues from humans far better than do wolves, their undomesticated ancestors. (Contrary research has recently been published by Monique Udell of the University of Florida and her colleagues.) Reid notes that Belyaev’s foxes, domesticated artificially, can follow pointing gestures as well as dog puppies of the same age, and are better at it than wild foxes. New Guinea Singing Dogs, similar to Australian dingoes, also perform of above chance, indicating that the ability to respond to human cues probably began in the earliest phases of domestication, since these unique dogs had only a rudimentary level of domestication before losing human contact. Perhaps dogs have learned to apply general rules of thumb such as “always approach the closest extension of the person,” or “always approach the person’s movement.” Such a mechanism would generally lead to the correct container in object choice tasks where a piece of food is placed in one of two or three containers and a human points to the correct container.

Reid attributes the third theory on the list above to the work of Adam Miklosi and Jozsef Topal and their colleagues, who argue that dogs and humans have evolved together to such an extent that human-like social skills have materialized in the dog in a process sometimes termed convergent evolution. This comes close to arguing that a dog understands that the human is trying to convey the location of food with a gesture. Miklosi has shown that dogs faced with an insoluble problem will look at a nearby human as though soliciting assistance. Reid argues that those scientists that take this “theory of mind” approach have found more sophisticated cognition in dogs than is justified by their research. It is, of course, likely that most pet owners would prefer to believe that there is a high level of human understanding in their pets.

Reid thinks the answer lies in the biological status of the dog as a scavenger, a niche that requires that an animal be acutely aware of other individuals in the social group that are also looking for opportunities to scrounge. They respond to our gestures towards food sources just as they respond to the other members of a pack that may be on the trail of a food source. This skill, combined with a tendency to learn, provided dogs with the skill to respond appropriately to our gestures, she argues. Reid admits that further research will be needed to narrow down the possible explanations as to why dogs are able to respond to our social cues. Pamela J. Reid, “Adapting to the Human World: Dogs’ Responsiveness to Our Social Cues,” 80 Behavioural Processes 325-333 (2009).