JOURNAL OF THE EXPERIMENTAL ANALYSIS OF BEHAVIOR 2008, 89, 247–261 NUMBER 2(MARCH)

A REVIEW OF DOMESTIC ’ (CANIS FAMILIARIS) -LIKE BEHAVIORS: OR WHY BEHAVIOR ANALYSTS SHOULD STOP WORRYING AND LOVE THEIR DOGS

MONIQUE A. R. UDELL AND C. D. L. WYNNE

UNIVERSITY OF FLORIDA

Dogs likely were the first animals to be domesticated and as such have shared a common environment with for over ten thousand years. Only recently, however, has this species’ behavior been subject to scientific scrutiny. Most of this work has been inspired by research in human cognitive psychology and suggests that in many ways dogs are more human-like than any other species, including nonhuman primates. Behavior analysts should add their expertise to the study of behavior, both to add objective behavioral analyses of experimental data and to effectively integrate this new knowledge into applied work with dogs. Key words: gestures, object permanence, theory of mind, social cognition, dogs ______

DOGS IN HUMAN SOCIETY the domestic dogs’ home environment, could play a crucial role in maximizing the quality of ‘‘That the dog is a loyal, true, and affectionate friend our interactions with dogs in a variety of must be gratefully admitted, but when we come to settings. consider the psychical nature of the animal, the limits Humans and dogs share a long intertwined of our knowledge are almost immediately reached’’ – history. DNA evidence suggests domestic dogs Sir John Lubbock. (1889, p. 272) most likely diverged from in different places at different times beginning as long as Our Intertwined Past 135,000 years ago (Vila et al., 1997). This is Sir John Lubbock’s opinion, outdated when the morphological structure of certain though its may be, is not an groups of wolves began to change to more inappropriate summary of the state of research closely resemble the modern domestic dog. Anthropologists and archaeologists have ar- on today. Domestic dogs are gued that this is an overestimate, claiming that never far away from most people’s lives, but the best way to determine the time of objective understanding of their behavior is domestication is to look for signs of a close still surprisingly scarce. association between dogs and humans (Morey, A better understanding of the variables 2006). One way this has been done is by controlling dog (Canis familiaris) behavior looking for evidence of dog burials. The could have practical importance for the earliest burial remains of a domestic dog are growing number of industries that utilize the 14,000 years old and were found in Bonn- behavior of domestic dogs—not only in formal Oberkassel, Germany (Nobis, 1979). The training settings, such as police dogs, drug- dimensions of the well-preserved lower jaw sniffer dogs, guide dogs, and so forth—but and teeth suggest that this animal was domes- also in the public realm, where the line ticated and could be compared to a small between the love of man’s best friend and sheep dog, making it the oldest known the fear of so-called ‘‘bad dogs’’ is a source of domesticated animal and a companion of the great anxiety. In addition, a more complete Cro-Magnon Man in the late Paleolithic age understanding of the role of social stimuli, (Nobis, 1979). The time line of dog burials which develops as a result of a natural history around the globe indicates the spread of dog of operant and classical conditioning within domestication at different geographic areas We thank Ray Coppinger, Leonard Green, Bill Roberts, (Morey, 2006). and John Staddon for most helpful comments on a previous draft. Role of Dogs in Human Society Address correspondence to Monique Udell and Clive Wynne, Department of Psychology, University of Florida, The exact location and lineage of the first Gainesville, FL, 32611. Email to [email protected]. domesticated dog are still under debate, but doi: 10.1901/jeab.2008.89-247 the impact that humans have had on the

247 248 MONIQUE A. R. UDELL and C. D. L. WYNNE domestic dog as a species is undeniable. Dogs reporting of dog attacks has been to label play an astonishing range of roles in human certain breeds as ‘‘bad dogs.’’ Malcolm Glad- society. Many individuals put their faith in well (2006) in the New Yorker likened the rescue dogs when stranded in the wilderness profiling of ‘‘dangerous dog’’ breeds to the or capsized in cold water. Others rely on guide racial profiling that has dominated the search dogs to get them safely to multiple destina- for terrorists since September 11th, 2001. As tions on a daily basis. Drug dogs, de-mining with most forms of prejudice and profiling, the dogs, police dogs, termite- and even cancer- banning of specific breeds of dogs from detecting dogs are trained and utilized as municipalities (most commonly at present substance detectors even in the face of the ), fails to effectively identify the competition from the latest technology. There environmental causes of undesired behavior so are herding dogs, hunting dogs, sled dogs, and that positive behavior can be reinforced and various other specializations that are crucial to aggressive behavior controlled with more the livelihoods of many individuals, not to enlightened methods. Breed profiling may mention the role dogs play in entertainment lead not only to a misguided fear of well- and the pleasures of individual dog owner- behaved dogs identified with a ‘‘bad’’ breed, ship—sufficiently reinforcing to sustain 74.8 but may also offer a false sense of security million dogs in the United States, at a cost to around a dog showing warning signs of their owners of over $100 billion (American aggression just because it comes from a breed Products Manufacturers Association, with a good reputation. 2007). However, qualities desired in one specializa- Phylogeny vs. Ontogeny tion may not be appropriate in dogs filling Despite the omnipresence of dogs in human another capacity. For example, the dependen- lives, scientific study of the factors that have cy on human guidance and direction sought in allowed dogs to thrive in human environments companion dogs may inhibit a rescue dog’s has until recently been surprisingly meager. ability to problem solve and function indepen- The causes of the characteristic behaviors of dently in situations when its handler is out of dogs can be understood at two levels. First are sight (Miklo´si, Pongracz, Lakatos, Topa´l, & the phylogenetic influences on behavior that Csa´nyi, 2005). It is important, therefore, to arise as a result of the unique evolutionary past take breed specializations and individual his- of domestic dogs. Second, and perhaps more tory into account when selecting dogs for importantly (at least in the sense that they are specific tasks. The more that is known about available for modification in real time), are the dog behavior, the more that can be done to ontogenetic causes that are the history of make the training of working dogs as efficient contingencies of reinforcement each domestic as possible. dog experiences within human society during A greater understanding of dog behavior its lifetime. also would be beneficial in a society that The phylogeny of dogs is particularly inter- perceives dog attacks and consequent deaths esting because, instead of natural selection by to be a growing problem. The Humane Society the environment, artificial selection by hu- of the United States estimates that 2% of the mans is responsible for the hundreds of breeds population is bitten by a dog each year (over of domestic dog that exist today. There is also six million people) and ten to twenty of these evidence that selection for desirable physical bites are fatal—with the victim usually a child and behavioral traits has led to many changes (Humane Society of the United States, 2007). in social behavior as unexpected byproducts Recently, the Minnesota Department of (Hare & Tomasello, 2005). This has led some Health (2007) reported a 40% increase in scientists to attribute the propensity of dogs the number of hospital treated dog bites for human social interaction to convergent between 1998 and 2005. According to attorney evolution, where the two genetically distinct Kenneth Phillips this increase in medically species were shaped by similar selective pres- treated dog bites is representative of an sures (Hare & Tomasello, 2005). increase in the dog population at large, which There is, of course, no question that genes rose 36% from 1986 to 1994 (Phillips, 2007). play a role in the behavior of domestic dogs, The public response to increased media but a dog’s individual environmental history DOMESTIC DOG BEHAVIOR REVIEW 249 plays a major role in shaping its behavior over reason (Darwin, 1871). Darwin also comment- its lifetime. From the time a is brought ed on how domestication impacted the behav- into a human household it is completely ior of domestic dogs, decreasing their fear of dependent on human caretakers for all of its humans, and he even argued for the evolution needs. The majority of reinforcers a dog will of distinct barks with various meanings. have access to throughout its life are con- Darwin’s neighbor in Downe, Sir John trolled, either directly or indirectly, by hu- Lubbock, was one of the first to carry out mans. This is comparable to the situation of experimental tests of the intelligence of dogs. young human children, and may explain in In the first recorded experiment on nonhu- part the similarities in sensitivity to human man language abilities, Lubbock trained his social stimuli shown by dogs and children. dog, Van, to bring him a card labeled ‘‘food’’ However, unlike children, domestic dogs by reinforcing this response with the presen- remain dependent on humans for primary tation of bread and milk upon retrieval. Once reinforcers, such as food, water, access to Van could readily discriminate between the mates, and even touch, throughout their ‘‘food’’ card and a blank card, Lubbock added lifetimes. Consequently, their access to rein- more cards containing words such as ‘‘out,’’ forcers is contingent upon appropriate behav- ‘‘bone,’’ ‘‘water,’’ and ‘‘tea,’’ and reinforcing ioral responses within the human social their retrieval with the action or item on the environment. Furthermore, behavior directly card. Although his data were, by his own related to subordinance and dependency is admission, preliminary at best, Lubbock re- often shaped in dogs from a young age. A ported that out of 113 card retrievals, Van puppy that sits by its bowl and whines for food selected the ‘‘food’’ card 80 times and the will usually have a greater chance of reinforce- ‘‘tea’’ card 31 times. Since the dog consumed ment than one who seeks out a source of food these items with alacrity, Lubbock concluded on its own, such as from a closet or off a table. that the dog had learned to communicate his Similarly, a dog that gets its leash or goes to wants effectively (Lubbock, 1889). Van’s suc- the door and barks when it has to relieve itself cesses inspired Lubbock to attempt to use this will likely be praised and be given the method to test the dog’s color discrimination opportunity to mark its , in addition abilities as well as its ability to count, but no to lessening the pressure in its bladder. A dog results were published. that urinates in the house, in contrast, is likely The most famous early researcher to use to receive punishment in the form of scolding dogs was, of course, . As is widely and in having its owner clean away its known, he discovered the form of condition- territorial scent. In this way, dependence and ing now associated with his name using sensitivity to human contingencies are shaped domestic dogs as experimental subjects. Pavlov quickly in domestic dogs in human house- exploited this phenomenon to explore dogs’ holds. In many cases reinforcement depends sensitivity to scents, touch, temperature, and on the dog’s ability to recognize social stimuli musical tones (Pavlov, 1906/1966). Less well presented by humans, both subtle human known is that he speculated on the role of gestures that may serve as discriminative Pavlovian conditioning in the training of stimuli for certain behaviors and overt mands domestic dogs: ‘‘You lift the dog’s paw saying which command a direct and specific response ‘give me your paw’ or even ‘paw,’ and then from the dog. give the dog something to eat. After repetition of this procedure the dog gives its paw at these words; it does so without any word of THE STUDY OF DOG BEHAVIOR IN command when it has a keen appetite’’ HISTORICAL PERSPECTIVE (Pavlov, 1936/1966, p. 309). The behavior of dogs was very important in the early history of . CURRENT DIRECTIONS IN Darwin wrote extensively about dog behavior, DOG RESEARCH intelligence and emotions, often using his own dogs as examples. He believed that dogs had The last twenty years have seen a resurgence emotions such as love, fear, shame, and rage, of research into the behavior of domestic dogs. as well as dreams, and the ability to imitate and Most of the studies reviewed here have drawn 250 MONIQUE A. R. UDELL and C. D. L. WYNNE their inspiration from work on developmental edly be shaped in many species through this and cognitive questions in humans and non- process over time, but dogs appear to demon- human primates. This search for common strate a sensitivity for human gestures that psychological processes in humans and dogs many other nonhuman species lack (Brauer, has been motivated by the fact that humans Kaminski, Riedel, Call, & Tomasello, 2006; and domestic dogs have shared a common Hare, Brown, Williamson, & Tomasello, 2002). environment and similar selective pressures Responses to gestures usually are tested in for tens of thousands of years. an object-choice paradigm. In this test, a reinforcing object is hidden in one of two or Responsiveness to Human Social Cues more locations or containers. The subject One of the most interesting behavioral enters the test area, and a gesture is given to characteristics of the modern domestic dog is indicate the location of the object. Alternative its predisposition to attend and respond to hiding places are equated for smell and other human social gestures and cues. Skinner cues and are usually sham-baited to control for (1953) noted that the behavior of other the effects of noise and human scent. The dog individuals can be an important source of is then allowed to approach the containers and social stimuli. Gestures and cues are social indicate a choice by touching or coming stimuli that likely started out as behaviors that within a required distance of one of the directly impacted the behavior of another locations. individual in a reinforcing or punishing way. Miklo´si, Polga´rdi, Topa´l, and Csa´nyi (1998) Skinner gives the example of a policeman’s carried out the first study investigating the use ‘‘stop’’ signal, which could have originated of human social cues by domestic dogs. from the action of a man putting out his hand Modeled primarily on studies with humans against another man’s chest forcing him to and nonhuman primates, two bowls were used stop. If this were aversive, the second man to hide food items in an object-choice para- might learn to stop before he reached the first digm. One of the bowls was baited out of sight man’s upheld hand in future presentations of the subject; the location of the food was (Skinner, 1986). Once a gesture is established, determined by a coin toss with no bowl being an individual’s history with the stimulus shapes baited more than twice in a row. The dog then his or her behavior in its presence. Thus, if the was led back into the room and was held social contingencies are established already for 3 meters from the bowls. The experimenter, behavioral responses to a particular gesture, who stood behind the bowls, made eye contact contact with the original behavior that evolved with the dog and then gave the predetermined into the gesture is not essential. Other gesture. The experimenter then returned to a examples of common human gestures include neutral position and the dog was allowed to pointing, nodding, reaching towards some- indicate its choice by approaching one bowl. A thing, or glancing between an object and correct choice resulted in food reinforcement another individual. Skinner focused on how and an incorrect choice ended the trial with gestures might come to act as social stimuli in no reinforcement. Five gestures were used in humans, but the basic principles could easily this study: pointing, bowing (bending the be applied to dogs as well. For example, if a upper torso), nodding, head-turning, and human throws a dog’s ball in a game of fetch, glancing with the eyes only. Each gesture was the throwing motion or outstretched arm presented a minimum of 30 times before the serves as a discriminative stimulus to chase next was introduced. All dogs experienced the something in the direction of the release. This gestures in the order given here. To progress reaction most likely ties into the reinforcing to the next gesture, 80% accuracy had to be effects of chasing a ball or catching prey along met for the previous condition. with the social reinforcers received for retriev- All 6 pet dogs in this study were able to use ing the object. This behavior, of following the pointing, head nodding, bowing, and head direction of an outstretched arm, may gener- turning to identify the target bowl without alize to less dynamic forms of the stimulus, and explicit training in the first fifteen trials, and the dog may begin to follow gestures such as the only significant initial difference among pointing or fake tosses to static objects to be dogs was the ability to use gazing as a retrieved. The use of gestures could undoubt- discriminative stimulus (Miklo´si et al., 1998). DOMESTIC DOG BEHAVIOR REVIEW 251

Subsequent studies have analyzed a wider set also sensitivity to context within a human of gestures and found dogs that can use, or be environment. trained to use, various types of pointing with This conclusion gains strength from recent the arm or extensions of the arm (Hare & research on the role of context in the training Tomasello, 1999; Miklo´si et al., 2005; Miklo´si of basic commands, such as ‘‘sit’’ and ‘‘come.’’ et al. 1998; Soproni, Miklo´si, Topa´l, & Csa´nyi, Fukuzawa, Mills, and Cooper (2005) demon- 2001; Soproni, Miklo´si, Topa´l, & Csa´nyi, 2002; strated that unintentional human cues influ- Udell, Giglio & Wynne, 2008), glancing ence how dogs respond after training. Dogs (Miklo´si et al. 1998; Soproni et al. 2001; Udell who responded to the commands ‘‘sit’’ and et al., 2007), local enhancement by a human’s ‘‘come’’ reliably when a human was giving the presence near the target (Hare & Tomasello, command, showed declines in performance 1999), and a human placing a token on a when the command was given by tape recorder target (Hare & Tomasello, 2005; Udell et al., in the human’s presence, and declined further 2008). when the human wore tinted sunglasses. Other studies of the exploitation of human Furthermore, when the human experimenter gestures by dogs have varied the way in which gave the two commands from behind a screen, conditions are presented. Instead of a hierar- out of sight of the dog, the dogs responded chical series of gestures in which one gesture dependably to the ‘‘come’’ command but not must be learned to criterion before the next is to the ‘‘sit’’ command (Fukuzawa et al., 2005). introduced, some studies have presented This finding makes sense when the context of conditions in orders that vary across subjects training and previous exposure is considered. and thus control for the effects of generaliza- ‘‘Come’’ is often applied and reinforced when tion from one gesture to another (Brauer et presented from a greater distance or when the al., 2006). Others have used probe methods to dog is out of sight, whereas the ‘‘sit’’ com- mand is usually given and reinforced only insert novel gestures into a series of trained or when the dog is in close proximity to the familiar gestures such as pointing (Soproni et human issuing the command. al., 2002). These studies have largely support- ed the conclusions from the pioneering work Ability to Cue Humans of Miklo´si et al. (1998), suggesting that Miklo´si et al.’s positive conclusions were not artifacts Most research in the area of social cues has of having the dogs master one gesture type focused on the dog’s response to human before proceeding to the next. gestures, but a study by Miklo´si, Polga´rdi, Particularly noteworthy in these studies of Topa´l, and Csa´nyi (2000) found that dogs that had seen a food item or a toy hidden in a dog responsiveness to human gestural cues, is specific bowl placed out of their reach while that some of the successful dogs in these their owner was out of the room, were able to studies had only had minimal contact with communicate to their owner the location of humans or did not live as in human the hidden target item when he or she households. Miklo´si et al.’s (1998) study returned. These dogs showed a significant included 5 assistant or guide dogs that did increase in mouth licking, vocalization, sniff- not reside in a typical household setting and ing, looking at the owner, and looking at the yet still performed above baseline in the location of the hidden object after the toy had pointing and bowing conditions in the first been hidden and the owner returned. Vocal- 15 trials. izations and gaze directed at the location of The degree to which individual dogs attend the hidden object were also higher when the to human social cues and their tendency to owner was present than when the dog was left rapidly integrate new behaviors into their alone after hiding, although both behaviors repertoire based on the consequences that occurred in both conditions (Miklo´si et al., follow from them, says something about both 2000). Gazing between the owner and the their development and their environment. For location of the food or toy occurred an average dogs to provide adaptive responses to human of three times in the first minute, with 8 out of gestures requires not only attentiveness and 10 dogs looking first at their owner and then at close proximity to human action, indicative of the location of the hidden item (Miklo´si et al., some sort of social attachment to humans, but 2000). This suggests that the dogs remem- 252 MONIQUE A. R. UDELL and C. D. L. WYNNE bered where the desired object was hidden Gagnon and Dore´ (1992) found that their after the person who hid it had left the room, dogs were more successful on the visible and that the dogs displayed behaviors, such as displacement tasks than on the invisible tasks, glancing between the naive owner and the but some dogs—those that experienced all location of the object, specifically instrumental four visible displacement tasks first before in getting the owner to uncover the target moving on to the invisible displacements— object. were then successful on the invisible displace- Dogs also follow the behavioral cues of other ment tasks. Unlike the studies of dogs follow- dogs in object-choice tasks. In one study, dogs ing human gestures, the data in most cases could find a hidden item at above-chance showed improvements across trials rather than levels when a trained demonstrator dog a spontaneous ability to follow the cues oriented towards the correct location while offered. gazing at it, or presented a local enhance cue This study is important within a Piagetian such as sitting by the correct location (Hare & framework because it showed that domestic Tomasello, 1999). The specifics of this study dogs could display behaviors characteristic of will be discussed later, but these findings may the sixth, and most advanced, stage of object suggest that this kind of ‘‘showing’’ or cuing permanence (Gagnon & Dore´, 1992).This behavior is part of the everyday behavioral conclusion, however, is not universally accept- repertoire of the domestic dog. ed. Other research has suggested that al- though dogs still search for the toy in invisible Object Permanence displacement tasks, they are not truly demon- ‘‘Object permanence’’ is a Piagetian term strating stage six behavior because their search for an individual’s continued interest in a patterns do not match those of children in stimulus after it has disappeared from sight. that stage (Watson et al., 2001). Furthermore, Children go through several stages of object a follow-up study provides evidence that dogs permanence during development, from a in these types of experiments are not showing complete disregard for obscured objects at object permanence at all. Collier-Baker, Davis, the earliest ages of testing, to sustained search and Suddendorf (2004) demonstrated that it for hidden objects starting around age 2 years. was the final resting place of the pole used to Dogs have been tested for object permanence move the target ball that cued successful of varying levels. Gagnon and Dore´ (1992) responding, not object permanence after all. completed a series of eight tests with 30 dogs of different breeds. The first four tests made Theory of Mind up the visible displacement task. In these tests Dogs appear to be sensitive to the attention- a toy was placed behind a screen in full view of al state of humans and this in turn has an the dog, and subsequently moved from screen impact on their behavior in a variety of to screen—but always so that the dog could situations. For example, in conditions where easily observe the movements. The last four taking a piece of food has been forbidden, tests made up the invisible displacement task. domestic dogs are much more likely to take In these tests the toy was first placed in a the food if the human experimenter does not container before it was moved. The container have a direct view of the food or of the dog with toy was then placed behind a screen, the approaching the food (Brauer, Call, & Toma- toy was inconspicuously removed from the sello, 2004; Call, Brauer, Kaminski, & Toma- container and left behind the screen, and sello, 2003). In conditions where the experi- finally the now-empty container was shifted menter has a clear view of the dog and the behind a different screen. The dog could not food, dogs typically obey the wait command know that the container was empty and would given by the experimenter. However, dogs naturally go to the container first. An individ- instructed not to take the food often disobey if ual that has mastered invisible displacements is the human’s eyes are closed, if the human’s one that, on finding the container to be back is turned, if the human is distracted, if empty, returns to the last place the container the human leaves the room, or if some barrier stopped to search for the toy. Reinforcement blocks the human’s view of the food and the in this study consisted of the opportunity to dog’s approach to the food (Brauer et al., play with the toy once it was found. 2004; Call et al., 2003). DOMESTIC DOG BEHAVIOR REVIEW 253

Gacsi, Miklo´si, Varga, Topa´l, and Csa´nyi foraging strategy based on the greatest chance (2004) concluded that the body orientation of reinforcement. and eye visibility of a human also has an effect on the begging behavior of dogs. Dogs were Word Learning given the opportunity to approach and beg In 2004 Science published a report of an from one of two women holding sandwiches. exceptional named . Rico In one condition the two women faced the could recognize vocal labels for over 200 items, dog: One with a blindfold on her head, and mostly toys, which he retrieved by name. the other with a blindfold over her eyes. In the Kaminski, Call, and Fischer (2004) demon- other condition one woman faced the dog and strated that Rico also was able to identify a tried to maintain eye contact without moving novel item from a group of familiar items and her head or body, whereas the other woman would retrieve the novel item in response to an faced away from the dog and ignored it. Dogs unfamiliar item name in 70% of trials. were given a piece of food no matter whom Exclusion learning and fast mapping were said they begged from in each trial. Nevertheless, to occur, and Rico was credited with not only in both conditions, dogs begged significantly pairing an unfamiliar name with a novel item more from the seeing or attentive individuals but remembering the new name for the novel than from the other woman. item in later testing sessions. Research of this kind often has been used in Rico’s vocabulary is certainly impressive and support of the possibility that dogs possess a suggests the potential dogs may have for ‘‘theory of mind’’ or ability to adopt the learning associations between items and hu- perspective of others (e.g., Brauer et al., man vocal cues. However, Rico’s ability to fast 2004; Gacsi et al., 2004). However, such map—or pair items with a novel name after performances also could be due to past one association—was far from perfect. When experience with similar contingencies. When he was given the name of one of the previously food is forbidden, taking the food while a novel items ten minutes after the first pairing, human’s face is oriented to the food and Rico retrieved the correct item out of a pile of visible to the dog would likely be punished. nine toys in four out of six trials. However, However, taking food in situations where the when tested an hour after the first pairings, human’s face is not appropriately oriented is using a different set of items, his performance more likely reinforced by obtaining the food dropped to retrieving the correct item in three and less likely to be punished. Furthermore, if out of six trials (Kaminski et al., 2004). begging from a person who is looking at a dog usually leads to reinforcement and begging The study with Rico raises interesting from someone who is not oriented towards the questions about the capacity dogs have for dog does not (as might occur at a family name learning and the amount of exposure dinner table), then reinforced begging behav- required to learn the names of new objects. ior directed towards attentive individuals But more research is needed before the should increase whereas nonreinforced behav- implications of his performance become clear. ior towards nonattentive individuals should Questions that remain open include: Is Rico decrease. Despite the fact that reinforcement an exceptional dog, or could his achievements was available for begging from either woman be replicated in other dogs given appropriate in Gacsi’s study, a long history of begging training? What might the necessary and would increase the probability of begging from sufficient training regimen be to train a dog an attentive person in the first place, and the to respond to vocal labels in this way? What is dog may never come into contact with the the limit of a dog’s vocabulary? How does a new contingencies. Furthermore, it is possible dog generalize to words pronounced in that a dog reared with different contin- different ways and by different individuals? gencies in place, for example one that only successfully obtains food when humans are not Individual and Breed Differences looking, would show the exact opposite It is a widely accepted part of the common behavior. In this case it is not the lore that different breeds of dogs show individual’s ‘‘theory of mind’’ which is at characteristic behavioral patterns and apti- stake, but rather the development of a tudes, and that individual dogs differ in their 254 MONIQUE A. R. UDELL and C. D. L. WYNNE temperaments. In an attempt to quantify these focused on our closest genetic relatives, lay impressions, Svartberg (2004) developed particularly . Though much re- the dog mentality assessment (DMA). The mains controversial in this field, it seems clear assessment consists of a battery of tests, such as that chimps and several other species of the dog’s reaction to social contact, play, chase primates are only modestly successful on many games, passive situations, strangers, sudden tasks designed to test for human-like social appearances of objects, and loud noises. reasoning. Thus, chimpanzees are only able to Factor analysis on these scores led to the follow gaze and show joint attention under a identification of six traits: playfulness, chase- limited set of conditions (Barth, Reaux, & proneness, curiosity/fearlessness, sociability, Povinelli, 2005). In the object-choice task aggressiveness, and distance-playfulness. Fol- described above, few chimpanzees or other low-up questionnaires indicated the stability nonhuman primates are able to use gaze or and value of the DMA for predicting broader other social cues such as pointing to identify personality dimensions, such as a placement the location of a hidden object (Call, Hare, & along a shyness–boldness continuum (Svart- Tomasello, 1998; Call & Tomasello, 1998; berg, Tapper, Temrin, Radesater, & Thorman, Itakura, Agnetta, Hare, & Tomasello, 1999; 2005). However, the DMA has been less Povinelli, Reaux, Bierschwale, Allain, & Simon, successful at identifying and predicting long- 1997; Tomasello, Call, & Gluckman, 1997). lasting aggressiveness and nonsocial behavior- Successful individuals typically need dozens of al problems (Svartberg, 2004; Svartberg et al., repeated exposures to the cue, and show poor 2005). transfer after even small changes to the testing Evidence for inherent breed and sex differ- environment (Brauer et al., 2006; Call, Ag- ences, as measured with the DMA, is limited. netta, & Tomasello, 2000; Itakura et al., 1999). One study indicated that high scores on the Dogs, in contrast, though they share much boldness scale do not correlate with the breed less of our genetic material than do chimpan- or sex of a dog. However, breed and sex zees, nonetheless show a spontaneous ability to appear to play some role for the lower scoring follow human gestures to find reinforcing dogs, of which female German Shepherds and objects, even in the absence of training in the other tested breed of , Belgian the laboratory. Most remarkably, even dogs Tervurens, scored lower than male German raised with minimal human contact can follow Shepherds (Svartberg, 2002). Furthermore, a a human point and gaze gesture without later study (Svartberg et al., 2005) indicated explicit training (Hare et al., 2005). that scores on all six personality traits did not Chimpanzees also have been the species vary significantly by breed types divided into most intensely studied for any ability to herding dogs, guarding dogs, and gun dogs. respond to the attentional state of humans or This is not to say that differences do not exist conspecifics—so-called ‘‘Theory of Mind’’ between individual breeds; however, the abilities. However, several published studies source of these differences does not seem to have failed to find any evidence of a sensitivity be explained by the current personality tests or to another’s knowledge (e.g., Brauer et al., models. More tightly controlled behavioral 2006; Povinelli & Eddy, 1996), and studies that methods, focusing on individual differences do suggest this ability (e.g., Hare & Tomasello, and specific behavior problems, may have 2004) have been subject to extensive criticism more success at getting to the root of the (e.g., Boesch, 2007; Heyes, 1998; Penn, Ho- environmental influences that shape these lyoak, & Povinelli, in press). Dogs, in contrast, differences in behavior. respond readily to human cues in these kinds of tests (e.g., Brauer et al., 2004; Call et al., DISCUSSION 2003; Gacsi et al., 2004). Chimpanzees have been by far the most Social vs. Causal Cues: The Difference Between Dogs intensively studied species for the comprehen- and Nonhuman Primates sion of human language (including seminal Ever since Darwin (1859), the search for studies by Gardner & Gardner, 1969; Savage- human-like social cognition (i.e., behavior Rumbaugh et al., 1993; Terrace, 1979), but no controlled by human and conspecific social peer reviewed paper has ever claimed the cues similar to that observed in humans) has rapid ‘‘fast-mapping’’ of language acquisition DOMESTIC DOG BEHAVIOR REVIEW 255 found by Kaminski et al. (2004) in the dog heightened responsiveness to human social Rico. stimuli (Hare et al., 2002; Hare & Tomasello, Several theories have been proposed to 2005). It also is possible that by removing explain why dogs perform so well on tasks genetic tendencies towards aggression and involving socially mediated stimuli. The possi- fear towards humans, other preexisting social bility that dogs learn to attend to human social behaviors were no longer blocked and thus cues simply because of the intensity of their could increase in frequency. interactions with humans appears to be refut- If selective breeding and domestication ed by the observation that even and serve as a likely explanation for the success of domesticated fox kits that have had only domestic dogs on tasks involving human social minimal exposure to human beings, nonethe- cues, then that begs the question—Why don’t less respond very accurately to human cues in other domesticated animals share these abili- choice paradigms (Hare et al., 2005). ties? In fact, domestic cats have been shown to Hare and Tomasello (2005) considered the be only slightly less successful than dogs in possibility that domestic dogs’ high sensitivity using basic pointing cues to find a hidden to social cues is an evolutionary legacy inher- food item in a simple choice test (Miklo´si et ited from wolves, the dog’s closest wild relative al., 2005). However, when presented with an and progenitor. If general social traits com- unsolvable task, where food was hidden in a mon to wild canids have simply been inherited butter pot but tied to a stool in such a way that by domestic dogs, then wolves also should do retrieval was impossible, dogs looked between well on tasks involving social cues. However, the problem and their owner more often and when compared to wolves and wild foxes, for longer periods of time, whereas cats only domestic dogs (including puppies) make occasionally looked towards their owners and significantly more correct responses on choice spent much more time trying to get the food paradigms where social cues serve as the themselves. This may indicate that: (1) During discriminative stimuli (Hare et al., 2002; Hare domestication cats were selected for traits less & Tomasello, 2005). This is true even though tied to the approach of humans and fear the wolves tested had been socialized and reduction, or (2) less stringent contingencies raised by humans in their homes as pets. Thus, exist for cats in their home environment it does not seem that domestic dogs simply leading to behavior that is more independent inherited the predisposition to attend to social of human action, or both. stimuli from wolves. The lower responsiveness and less frequent Hare and Tomasello’s (2005) study includ- orientation of cats to human cues may in fact ed, alongside tests on domestic dogs, compar- be related to the fact that domestic cats are ison tests on fox kits that had been selectively closer to their wild relatives than dogs are to bred over 46 years for nonaggressive behavior wolves. The domestic cat (Felis catus) shows towards humans. These fox kits were com- only a low level of genetic divergence from its pared to others reared under the same two nearest wild relatives (the European conditions but not selectively bred for low wildcat, F. silvestris, and African wildcat, F. aggression. Neither group of foxes had been libyca), and the earliest evidence for cat domes- raised in human homes (nor had the earlier tication is only around 8,000–9,500 years BP— generations from which they were descended). considerably more recent than that for dogs Hare and Tomasello found that the fox kits (between 14,000 and 135,000 years BP) (Dris- bred for nonaggressive reactions to people coll et al., 2007; Serpell, 2000; Vigne, Guilaine, performed just like domestic dog puppies on Debue, Haye, & Ge´rard, 2004). The traits pointing and gazing tasks. The fox kits that selected for in the domestication of the two had not been selectively bred performed species also may have led to differences in the poorly on these tasks, at a level similar to that responsiveness and attentiveness each has seen in wolves (Miklo´si et al., 2003). towards humans. Even today, many dog breeds These results suggest that during domesti- are selectively bred to work in close association cation, traits that were often selected by with humans, filling specific roles in industries humans, such as lack of aggression and such as farming, therapy, police, and search- fearlessness towards people, may have carried and-rescue. Even with earlier partnerships with them other genetic traits that led to a such as hunting it is quite probable that a 256 MONIQUE A. R. UDELL and C. D. L. WYNNE dog that stayed close to its owner or was quick were nursed by the same mother until to respond to its owner’s actions would have weaning, at which point they were hand raised been a more beneficial working companion, and fed by humans. securing its place in the group and ultimately The wolves reached several physical devel- in the gene pool. opmental landmarks days ahead of the mala- Cats were likely used as mousers and kept as mutes. For example, the wolf pups began pets from early in their domestication (Vigne climbing over their 45-cm pen wall at only et al., 2004), but they are not typically bred for 19 days, whereas the malamute pups could not purposes that require a close partnership with climb over their 15-cm den box opening at humans, even today. Thus, a house cat’s 32 days old. However, socialization of the independence could have actually been a wolves was much more difficult than of the beneficial trait that increased the chances of malamutes. At 2 weeks of age the wolf pups its survival in the same environment. Further- avoided the human handlers whenever possi- more, cats are often chosen as pets because ble and hid behind the wolf dam when they are considered low maintenance com- humans approached. At 6 weeks they became pared to dogs. They do not require walking, less fearful but somewhat indifferent to the they sleep or entertain themselves most of the human presence, preferring to be around day, and they are typically small and quiet adult wolves or dogs in the enclosure. The enough to go unnoticed much of the time. malamutes, in contrast, became more inde- Thus, there are many more opportunities for pendent of the nursing wolf, and actively cats to engage in independent behaviors approached nearby humans and engaged in without immediate human consequences with- ‘‘greeting frenzies’’ on a regular basis (Frank in the home environment. & Frank, 1982). Several studies have looked for key similar- However, this study has some potential flaws. ities and differences between wolves and dogs. First, all of the pups were raised by a wolf foster Perhaps the most striking developmental mother, which could have potentially impact- difference between dogs and wolves is that, ed the behavior of the mother to the foster whereas dogs can be socialized to humans pups or the behavior of the growing pups within the first sixteen weeks of life, wolves toward the foster mother. Without a compar- must be removed from their mother for ison using a Malamute foster mother for both human socialization before fourteen days of species it is impossible to say that having a age, or acceptance of humans is very unlikely same-species foster mother would not produce (Klinghammer & Goodman, 1985). a closer bond to that individual and therefore less of a bond towards humans. Second, since Implications for Phylogeny and Ontogeny the two groups of pups were raised at different In a study by Frank and Frank (1982), times, other factors may have been present in domesticated dogs (Alaskan malamutes) and one study that were not accounted for in the wolf pups that were raised in identical condi- next, for example, the age of the foster mother tions in a home environment showed distinct or other canine group members and the differences in both physical and social devel- previous experience of the experimenters opment. Conducted as a two-stage experiment, raising wolfs before raising the Malamutes. 2 malamutes acquired at 10 days old were To address some of these concerns, Kubinyi, compared to 2 wolf pups acquired at 11 days Viranyi and Miklo´si (2007) conducted a old a year before. The wolf and dog pups did similar study comparing the development not interact, but the conditions were kept and behavior of wolf pups and dog almost identical for the two groups during the pups in foster homes with human caretakers. experiment. Interestingly the two major dif- In this study, all pups were individually ferences were that wolves were given more assigned to a human caretaker who hand socialization to humans, as they were required raised and fed his or her pup from 4 to 6 days to sleep with their human foster parent two old. Both sets of pups participated in multiple out of every three nights as pups, and the behavioral tests from 3 to 9 weeks of age. malamutes, who did not receive this extra When the wolves reached 9 weeks of age they socialization, were given slightly more frequent had to be integrated into a captive wolf , exposure to the outdoor enclosure. All pups but were still visited by their caretakers at least DOMESTIC DOG BEHAVIOR REVIEW 257 once or twice a week. Unfortunately the the two species lived in such close proximity mongrel dogs in the study continued to live over 10,000 years. It also is the case that it in a human household at this point, so testing would have been beneficial to humans to later in their lives could have been impacted create similar or complementary social traits by different home environments. Nevertheless, in these animals through selective breeding. the study found that the wolves could be Of course, over most of this history of artificial handled by their caretakers similarly to dogs selection, the human breeders would have when tested between 1 and 2 years of age. This understood nothing of genetics or selective included coming when called, sitting and lying breeding. Simple operant conditioning would down on cue, allowing dog accessories such as be sufficient to explain the selection of dogs a muzzle to be put on, and minimal social and with desirable traits. Dogs that bit or attacked a physical neophobia. The level of attachment, human may have been killed, whereas ones measured by the length of time the wolves that worked well with humans on the hunt and spent in close proximity to their caretaker at 1 were nonviolent to their owners were taken to 2 years of age, however, was less for wolves care of and had a greater chance of reproduc- than it was for the dogs. The domestic dogs tive success. Over time, people would have also out-performed the wolves on tasks involv- learned to recognize traits in puppies that had ing more complex human social cues, such as typically led to aggressiveness in older dogs in momentary distal pointing. The wolves could the past, and the process of selecting desired be taught to use the same level cues as the individuals and rejecting ones with undesir- dogs at 11 months, but only after extensive able traits would have become more efficient. training (Kubinyi et al., 2007). In other words, the selection of particular Studies comparing domestic animals and traits in dogs would be reinforced with the their closest genetic relatives are a good step in presence of cooperative, nonaggressive dogs, the direction of identifying the role phylogeny whereas the tolerance or selection of other and ontogeny play in key behaviors that traits might be punished with aggressive seemingly make the species behaviorally dis- attacks or a lost investment of food and energy tinct. However, much care needs to be taken if a fearful dog runs away. to make sure both species are treated equiva- Of course, phylogeny may set the limits of lently and that the behavior that results is not a what is possible in behavior, but it is ontoge- byproduct of some unintended aspect of the ny—the personal history of reinforcement— experimental environment. This includes tak- that determines what an animal actually does. ing into account genetic and developmental In a study by Hare and Tomasello (1999), differences that may impact how different domestic pet dogs demonstrated the ability to species respond to stimuli when presented at use the location and gestures of both humans the same age or in different environments. and other dogs to help locate hidden food. The fact that various domesticated animals Four conditions were used: human–local do better than their nondomesticated relatives enhance (the human squatted by the correct on tasks requiring the use of human social location); dog–local enhance (another dog sat stimuli indicates that selective breeding and by the location); human–gaze- and-point; and domestication play some role in this class of dog–gaze-and-point (the other dog faced and behavior. These genetic traits or predisposi- looked towards the location). When perfor- tions may have been a result of artificial mance was assessed as a group, the 10 subject selection in some species, but they are still a dogs in the study found food significantly product of the evolutionary history of that more often in each of the experimental species. Instead of mountains creating the conditions than in the control or baseline geographic isolation of a pack of wolves, stone condition where no cue was provided. As a walls and chains may have determined which group, no one condition appeared to be more individuals could breed. In place of a natural helpful than another. However, individual distribution of ecological resources, a human dogs differed greatly in which stimulus they hand may have determined which individuals were most successful in using to find the target would live or die within a pack. location. Only 2 dogs were successful in all Dogs may have developed at least some four conditions, 1 dog was successful in three behaviors similar to those of humans because conditions, 2 dogs were successful only with 258 MONIQUE A. R. UDELL and C. D. L. WYNNE the human communicator, 2 only with the dog some owners seek out breeds that have a communicator, 1 during both the human– reputation as ‘‘bad dogs’’ and then shape the and dog–local enhancement conditions only, aggressive behaviors that later seal their fate. and 2 during the human–local enhancement According to Randall Lockwood, a senior vice- condition only. These differences are most president of the ASPCA, ‘‘A fatal dog attack is likely due to different levels of experience in not just a by a big or aggressive dog. It the home with situations similar to the ones is usually a perfect storm of bad human–canine the experimenters set up in the laboratory. interactions—the wrong dog, the wrong back- ground, the wrong history in the hands of the Dog Profiling Revisited wrong person in the wrong environmental If, then, there is a genetic component to situation’’ (cited in Gladwell, 2006, p. 26). some aspects of behavior that have a clear Dogs may become problems in human impact on human–dog interaction, can bans society because their owners may also respond targeting ‘‘bad dog’’ breeds such as pit bulls, or in unconventional ways to social stimuli within profiling based on genes in general, be justified the environment because of their own histo- by maintaining the position that behavior is a ry—possibly exposing their dog to contingen- product of genetic tendencies as well? Evidence cies governed by an abusive, isolated, or suggests that the answer is no. Although bites neglectful home environment. Therefore, to and deaths attributed to pit bulls are up in fully address these and other types of behav- recent years (Sacks, Sinclair, Gilcrist, Golab, & iors demonstrated by domestic dogs, the Lockwood, 2000), other breeds have been specific contingencies that surround the oper- number one for aggression against humans at ant and the specific properties of social stimuli other times. German shepherds and St. Ber- that serve as effective discriminative stimuli nards were estimated to be responsible for the need to be identified and defined. majority of deadly dog attacks, not including police dogs, from 1975 through 1980 (Pinckney Dogs: Our Closest Relatives? & Kennedy, 1982). In the 1970s, Dobermans It may sound strange, but it is not unrea- were on the top of the list (Randall Lockwood sonable to view dogs and humans as subject to of the ASPCA, as cited in Gladwell, 2006), and convergent evolution (Hare & Tomasello, between 1993 and 1998 Rottweilers were the 2005). Over the last 100,000 years, the social most dangerous (Sacks et al., 2000). environments of domestic dog pups and However, these estimates are imperfect because human children have become more and more they do not take into account the baseline similar to each other, and less like those of populations of each breed in the U.S. at any either species’ closer genetic kin. given time, and identifying an individual as a It is as a consequence of this intense specific breed is not always clear cut. Therefore, cohabitation that dogs have come to emulate breeds that have a larger population may be involved in more attacks than less popular some behaviors that are commonly viewed as breeds but proportionally may be less aggres- uniquely human, such as the recognition of sive; and aggressive dogs that do not fall clearly another’s attentional state. These kinds of into a breed category are often labeled as a complex behaviors are commonly structured breed that is already deemed aggressive, there- in relatively vague cognitive terminology. We by inflating the numbers for that breed. hope this review will inspire behavior analysts However, even in times where one breed may to use the empirical tools of our field to show proportionally higher levels of aggressive investigate just how closely dog social behavior behavior, there is evidence that this is not solely maps onto human use of social cues. Such due to an inherited ‘‘bad dog’’ gene. In fact, research could answer fascinating questions in the type of owner, not the breed of the dog, is the evolution of complex behavior, as well as the best predictor for dog attacks (Gladwell, enabling us to live more safely and profitably 2006; Siebert, 2004). In a quarter of fatal dog with our ‘‘best friends.’’ attacks, the owners previously had been arrest- ed for illegal fighting, and many aggressive dogs To Shape, Lead, Catch, or Click? are ones that have been abused, starved, or The study of dog behavior may seem new to deprived of medical attention. In addition, experimental behavior analysis, but the inter- DOMESTIC DOG BEHAVIOR REVIEW 259 est in applying behaviorist technology to dog Brauer, J., Call, J., & Tomasello, M. (2004). Visual training dates back to Skinner’s own writings. perspective taking in dogs (Canis familiaris) in the presence of barriers. Applied Animal Behaviour Science, Skinner wrote: ‘‘Since nearly everyone at some 88, 99–317. time or other has tried, or wished he knew Brauer, J., Kaminski, J., Riedel, J., Call, J., & Tomasello, M. how, to train a dog, a cat, or some other (2006). Making inferences about the location of animal, perhaps the most useful way to explain hidden food: Social dog, causal . Journal of Comparative Psychology, 120, 38–47. the learning process is to describe some simple Call, J., Agnetta, B., & Tomasello, M. (2000). Cues that experiments which the reader can perform chimpanzees do and do not use to find hidden himself’’ (Skinner, 1951/1999, p. 605). He objects. , 3, 23–34. went on to provide techniques to shape the Call, J., Brauer, J., Kaminski, J., & Tomasello, M. (2003). Domestic dogs (Canis familiaris) are sensitive to the behavior of any animal the reader could attentional states of humans. Journal of Comparative ‘‘catch’’ using the basic principles of positive Psychology, 117, 257–263. reinforcement (Skinner, 1951/1999). Three Call, J., Hare, B., & Tomasello, D. (1998). gaze decades later, Karen Pryor reintroduced be- in an object choice task. Animal Cognition, 1, 89–99. Call, J., & Tomasello, D. (1998). 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