An overview of the dog–human dyad and ethograms within it

An overview of the dog–human dyad and ethograms within it

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  POINT-COUNTERPOINT  An overview of the dog–human dyad and ethogramswithin it Paul D. McGreevy a , Melissa Starling a , N. J. Branson b , Mia L. Cobb c,d , Debbie Calnon e a Faculty of Veterinary Science, University of Sydney, Sydney, NSW, Australia; b  Research Services Division, Deakin University, VIC, Australia; c Guide Dogs Victoria, Kew, VIC, Australia; d   Anthrozoology Research Group, Monash University, VIC, Australia; and  e  Behaviour Counselling Service, Oakleigh South, VIC, Australia. KEYWORDS: dog–humaninteractions;intraspecificcommunication;interspecificcommunication;dominance;submission;deference Abstract  This article reviews the literature on the complex and variable nature of the dog–human dyadand describes the influence of terms such as ‘‘dominance’’ on attitudes that humans have toward dogs.It highlights a legacy of tension between ethology and psychology and notes that some practitionershave skills with dogs that elude the best learning theorists. Despite the widespread appeal of being ableto communicate with dogs as dogs do with one another, attempting to apply the intraspecific dog etho-gram to human–dog and dog–human interactions may have limited scope. The balance of learning the-ory and ethology on our interactions with dogs is sometimes elusive but should spur the scientificcommunity to examine skills deployed by the most effective humane practitioners. This process willdemystify the so-called whispering techniques and permit discourse on the reasons some trainingand handling techniques are more effective, relevant, and humane than others. This article exploresthe mismatch between the use of nonverbal communication of 2 species and offers a framework forfuture studies in this domain. Technologies emerging from equitation science may help to disclose con-fusing interventions through the collar and lead and thus define effective and humane use of negativereinforcement. The case for a validated intraspecific and interspecific canid ethogram is also made.   2012 Elsevier Inc. All rights reserved. Introduction In the 17th century, English law viewed animals as guilty of their actions. For example, ‘‘When in 1679 a Londonwoman swung at Tyburn for bestiality, her canine partner incrime suffered the same punishment on the same grounds.’’By the end of the 19th century, the law had changed to viewanimals as the property of their human owners, and itremains this way in many countries today. As science beganto reveal that nature could be subject to human control, theperception that people were vulnerable to the metaphoricalmystique of animals was rationalized under the banners of zoology, taxonomy, and veterinary science. The accompa-nying shift in the nature of the relationship between humansand animals that remains today is that animals becameobjects of human manipulation. For a detailed review of thesocial domination of animals in the Victorian era, we referthe reader to the study by Ritvo (1990).Since the first half of the 19th century, the sentimentalvalueofcompaniondogshascontinuedtoincrease.Atitsbest, Address for reprint requests and correspondence: Paul D. McGreevy,BVSc, MRCVS, PhD, Faculty of Veterinary Science (B19), University of Sydney, Sydney, NSW 2006, Australia; Tel: 1 61 2 9351 2810; Fax: 1 612 9351 3957.E-mail: 1558-7878/$ - see front matter    2012 Elsevier Inc. All rights reserved.doi:10.1016/j.jveb.2011.06.001 Journal of Veterinary Behavior (2012) 7, 103-117  the dog–human relationship is characterized by strong at-tachment and the optimal well-being of both dogs (Kotrschaletal.,2009)andhumans(Barkeretal.,2003).Atitsworst,the dog–humanrelationshipisassociatedwithanimalabuse(foracomprehensive review, see Ascione, 2008) and the routinedestruction of unwanted and abandoned dogs (McGreevyand Bennett, 2010). Canine behavior problems can have anadverse effect on the well-being of owners and on the widercommunity (Voith, 2009), whereas the abandonment or loss ofcompanionanimalscanalsobeassociatedwithhumanpsy-chopathology(Hunt etal.,2008). For thesereasons,harmonybetween the 2 species is of critical importance.To better understand canine social behavior and, in turn,the dog–human dyad, we do well to first study the ways inwhich social harmony is created and maintained in stablegroups of dogs. The peacefulness that usually defines suchestablished dog communities reminds us that there are veryfew breaches of social order and that aggression is rare(Bradshaw et al., 2009). This is underpinned by clear signal-ing and deference, delivered not demanded (Overall, 1997).Rough physical contact is far more often part of play thanof violence, and it is foreshadowed by strong signals(Horowitz, 2009a).This article will review the literature relating to ourcurrent understanding of the complex nature of the dog–human dyad and examine its characteristics. First, it con-siders the srcins of social-domination belief systems andhowsocialorderisusuallystudied.Second,itreviewscaninesocial behavior and social learning. Third, it examinescanine–human interactions, examining the extent to whichthey reflect or are informed by the canine ethogram and bylearning theory. We summarize by exploring our ability toapply the canine social ethogram to handling and trainingandtoassess thelimitations ofthisapproach, andwe suggestthat it is possible to estimate the contribution of ethologicaland psychological principles in the manifestations of certainresponses. However, the emphasis here is on estimation, weare not suggesting that we can quantify the absolute roles of learned rather than innate responses. Context can determinewhether learning theory will have a greater influence or bemore informative than ethology when training and handlinganimals (McGreevy et al., 2009); thus, we avoid using cuesof ethological significance if they run counter to a giventraining outcome. For example, because it so reliably trig-gers playful responses rather than conditioned responses,play-bowing (an innate canine meta-signal for play) is rarelyused as a visual discriminative stimulus in training. Usingthis approach, we offer a framework that helps to describethis effect in dog–human interactions. Origins and implications of the social dominancebelief system Social order can be understood as the product of dynamic and situation-specific relationships betweenmembers of a social group (Petherick, 2010). Social organi-zation in  Canis familiaris  can be studied by observing theway in which dogs gain access to and retain resources(Drews, 1993). Dominance is characterized as an aspectof a relationship between 2 or more animals in a socialgrouping rather than an attribute or trait of an individual.The ‘‘dominant’’ animal is considered to have higher statusover another or others in the group (Petherick, 2010). Adominance relationship involves a simultaneous expressionof both dominance and submission (Schenkel, 1967). Adominance relationship can be established without anysign of aggression only indicated by a submissive orappeasing posture from one of the protagonists. An appeas-ing attitude from the dog toward humans may thereforeindicate a man–dog dominance relationship. An individualdog’s motivation to gain access to a particular resourcemay be subject to some flux (Bradshaw et al., 2009)and resource-holding potential may be context-specific(Shepherd, 2002), but this should not demean its impor-tance. The ability to learn is similarly context-specific(McGreevy and Boakes, 2007). It is clear that dogs viewhumans differently from the way they view other dogs(e.g., Rooney et al., 2000). Nevertheless, we would dowell to study the role of intraspecific canine social interac-tions in dog–human interactions and human–dog interac-tions, if for no other reason than that humans areregularly bitten by dogs defending certain resources. Ag-gression is defined as deliberate threat and/or attack compo-nents of agonistic behavior with potential to cause injuryassociated with conflict and competition (Brain, 2010).Recent data suggest that higher scores for owner-directedaggression are associated with male dogs and femaleowners (Hsu and Sun, 2010), but this does not necessarily indicate social dominance as a cause. It is critical that therole of testosterone in impulsive and reactive aggressionamong companion dogs is better understood. And onlywhen we study how aggression and successful affiliativeactivities (such as play) (Horowitz, 2009b) emerge indog–dog dyads, will the subtleties of dog body languageand our ability to offend our canine companions, howeverinadvertently, become clear.Social order helps animals within a social group learnwhich of them can defend resources and displace anotherfrom them (McGreevy, 2004). This learning is underpinnedby communication and effectively reduces aggression(McGreevy, 2009). It can exist without the necessity forindividuals to have a sense or concept of their own status.Humans have gone to great lengths to interpret animalbehavior in terms of social order. Some of the theoreticalconstructs that have arisen in the process, such as ‘‘domi-nance,’’ have acted as obstacles to successfully extendingour understanding of animal behavior (Friedman andBrinker, 2001). Many authors (e.g., Semyonova, 2003) crit- icize labels such as ‘‘dominance’’ because they evokeemotional responses in the observer and can prejudiceinterpretations, interfere with verifiability of behavioral 104 Journal of Veterinary Behavior, Vol 7, No 2, March/April 2012  responses, and are tightly bound by the human perspective.It is important to note here that social dominance order (ororientation) is a term used in psychology to describe apersonality variable that predicts social and political atti-tudes. It is distasteful to many because it reflects an individ-ual’s preference for inequality among social groups (Prattoet al., 1994) and may in some ways relate to right-wingauthoritarianism.Non-Western philosophical frameworks, such asBuddhism, believe that animals exist in their own right,rather than as property, as they are represented in Westernlaw. Thus, it is pertinent to assess the validity of thedominance construct in terms of Western culture’s sanctionof the control of man over nature (Misra, 1995).In addition to the effect of cultural attitudes, it is alsoworth considering the potential effect of inattentionalblindness on human perception of dog behavior. Inatten-tional blindness is the notion that ‘‘we rarely see what weare looking at unless our attention is directed to it’’ (Mack,2003). This concept highlights the intimate link betweenour perception and our attention. Steinker (2007) arguedthat by labeling a dog as ‘‘dominant,’’ the humans involvedbegin to interpret many behaviors as evidence of ‘‘domi-nance’’ and ignore any evidence to the contrary. The con-cept of inattentional blindness may further assist withunderstanding why people are very likely to see, remember,and interpret dog–dog and dog–human interaction in termsof the dominance framework with which they are familiar.This concept illustrates the power of our intentions in deter-mining what we see and what we do not (Mack, 2003).On a practical level, it is clear that some practitionershave skills with dogs that elude the best learning theorists;they may insist that they are using canine ethology andimposing canine social order to communicate with dogs. Asa result, the role of dog owners and handlers as leaders,alphas, and trainers is widely debated. A popular view thathas, until recently, prevailed in dog-training circles is thatdog–dog interactions mirror wolf–wolf interactions. Anexample is provided by Bauer and Smuts (2007), whostated that ‘‘as studies of captive wolves found that posturalasymmetries were consistently unidirectional within dyadsand that dominance hierarchies based on these posturesshowed a high degree of linearity  .  such postures weretherefore considered reliable indicators of dominance forour purposes’’ (in studying companion dogs). These authorsthen went on to draw conclusions about play behavior incompanion dogs on the basis of their relative social status,which were based on wolf data.Bradshaw et al. (2009) reviewed data available on socialhierarchy in the dog from the perspective of dominancehierarchy. It seems that, historically, the suggestion thathumans could and should adopt the role of pack leader wasbased on 2 implicit assumptions: first, wolves are the ances-tors of domestic dogs, and second, that a linear hierarchyexistsinwolfpacks(vanKerkhove,2004a;2004b).Although the first point is widely accepted, the second has beenchallenged (reviewed by [Bradshaw et al., 2009; Semyonova, 2003; van Kerkhove, 2004a; 2004b; Steinker, 2007]).Themeritsoftheputativelinearhierarchyofwolfso-cial order as an appropriate model to apply to the social be-havior of domestic dogs has been widely discussed (vanKerkhove, 2004a; 2004b; Scott and Fuller, 1965; Serpell, 1995; Bradshaw et al., 2009; Steinker, 2007). Mech (1999) described 13 years of studying the socialorder within wild wolf packs, and the results of thisresearch contradict most of the widely held beliefs regard-ing dominance hierarchies in this species that have beenassumed to be applicable to the domestic dog. He foundthat family groups, rather than a linear hierarchy, wereobserved in wild wolf populations. Based on these results,van Kerkhove (2004a; 2004b) and Yin (2009) have sug- gested that ‘‘wolf pack theory’’ does not apply to domesticdogs and challenged the idea that humans should maintainsocial stability in their interactions with dogs by adopting a‘‘top-dog’’ role. Furthermore, Coppinger (2001) has arguedthat dogs are not pack animals. That said, there is evidencethat, where resources are sufficient, large groups of dogscan occupy a single area with minimal conflict (Bradshawet al., 2009) and that dogs can cooperate in tasks(McGreevy, 2009).Scott and Fuller (1965) believed that social hierarchieseffectively reduce and minimize overt aggression betweenindividual members of the pack but noted that a linear hier-archy does not seem to be a factor for the domestic dog inmaintaining social harmony. They evaluated social order intheir study using a ‘‘dominance test’’ on puppies at 5, 11,and 15 weeks of age. Two puppies were placed in a penwith a bone for 10 minutes. Dominance was defined as acondition in which 1 puppy kept possession of the bonefor at least 8 out of 10 minutes. The dogs were rated as‘‘dominant,’’ ‘‘incompletely dominant,’’ and ‘‘subordinate,’’and the effect of dominance on the amount of fighting wasassessed. The observations varied across 3 breeds: Foxterrier, Basenji, and Shetland sheepdogs. Breed differenceswere found in the association between ‘‘dominance’’(defined as control over a bone) and an effective controlsystem over fights between individuals. Thus, the notionthat dominance order could control fighting was upheld in2 of 3 breeds of dogs when observed between 5 and15 weeks of age. However, if we place these findings inthe context of the difficulty other scientists face whenattempting to develop tests in puppies that predict theirbehavior as adults (Wilsson and Sundgren, 1998; Battet al., 2009), we can only speculate how any associationbetween dominance and fighting might vary in dogs of other ages, let alone in other breeds.Scott and Fuller (1965) described 9 fundamental behav-ioral systems for dogs (investigative behavior, epimeleticbehavior, et-epimeletic behavior, allelomimetic behavior,agonistic behavior, sexual behavior, eliminative behavior,ingestive behavior, and comfort-seeking behavior [shelter-seeking]). They concluded that not only were these relevant McGreevy et al Overview of the dog–human dyad 105  to dogs of all breeds, they were also relevant as a frame-work for comparing human and dog behavior patterns.While acknowledging that, in many ways, dogs and humansare different in terms of anatomy, physiology, and behavior,these authors noted that social behavior patterns are similarenough, in many contexts, to be mutually recognizable.A brief consideration of analogues of dog–dog interac-tions that arise in human–dog dyads suggests that there areat least some human–dog interactions that align with thecanid intraspecific social ethogram. Analogues, such asallogrooming, can be useful for humans needing to groomdogs (McGreevy et al., 2005), whereas others may raisechallenges because there can be tension between ethologi-cal and psychological constructs in training. For example,although gaze-averting is a deference display in dogs(Vas et al., 2005), during some training sessions, it is critical to keep a dog’s attention focused on the handler.Furthermore, breed differences in attention to human cueshave been demonstrated (Ga´csi et al., 2009a), and differ-ences in aloofness (McGreevy, 2007a) and even retinalanatomy (McGreevy et al., 2004) may account for thelack of attention some dogs pay their handlers.Vas et al. (2005) developed a scale for assessing behav-ioral responses of dogs to approaches by unfamiliarhumans. These authors note that humans may have selecteddogs based,  inter alia , on variation in monitoring of andresponse to human cues. Certainly, this could be a firststep in selecting dogs that may excel at protection, guard-ing, and herding, all of which share related behaviors.Dogs have been selected for adaptations to human sociallife, and these adaptations have led to marked changes intheir communicative, social, cooperative, and attachmentbehaviors toward humans. In a review of canine socialcognition, Miklo´si et al. (2004) state that through a complexevolutionary process, dogs became adapted for living inhumansociety.Therefore,thehumanenvironmentandsocialsetting now represents a natural ecological niche for thisspecies. Dogs are extremely flexible in how they processspatial information and can simultaneously use cues fromdifferent sources and rank the cues based on the complexityof the environment (Fiset et al., 2000, 2006; Fiset and LeBlanc, 2007). If humans are part of that environment, wemust consider that dogs trained to work in the presence of humans who issue discriminative stimuli may disregardinformation that they, themselves, collected (Szetei et al.,2003). Given that companion dogs behaved differently(attempted a forbidden task) when the owners were in theroom compared with when they were not in the room(Schwab and Huber, 2006; Horowitz,2009b), itseems likely that intimate human–dog relationships (as occur in compan-ion dogs) may predispose dogs to behave in a sociallydependent manner. All of this suggests that canine scientistsseeking to advance communication in the dog–human dyadmust grant ethologically relevant mechanisms as muchattention as mechanisms that align with learning theory(McGreevy and Boakes, 2007). Studying domestic canid social order  Bradshaw et al. (2009) posit that resource holding poten-tial (Parker, 1974) may be less applicable to dogs than toother species, but that nevertheless it is useful because itoffers the concept of subjective resource value as a factorinfluencing the escalation of conflicts. Bradshaw et al.(2009) propose that the subjective resource value, in com-bination with associative learning, explains antagonisticencounters between dogs more simply than traditionaldominance theory. This is a useful contribution to explainresource-related aggression but it fails to either acknowl-edge the possible role of personality dimensions or explainthe mechanisms of dog–dog antagonistic interactions in the absence  of clearly disputed resources.It could be argued that encounters between 2 membersof a dyad are never resource-neutral. Fighting may beexhibited in different contexts, including competition overa resource, and contexts not clearly related to resourcepossession (Hahn and Wright, 1998, cited by Wright, 2004). For example, when dogs first meet, one of them ismore the territory holder than the other (even if only byvirtue of being on that site for longer than the protagonist)and perhaps presence on the territory is a quasi-resource.But when meeting for the first time, how can dogs besure they are valuing or fighting over the same resource?Before any associative learning about their relationshipcan take place, their behavior may represent a manifesta-tion of positive and negative personality dimensions suchas those described by Sheppard and Mills (2002) or the5 personality factors described by people interviewed inthe study by Ley et al. (2007).A given dog’s ability to impose social status at the firstmeeting would seem to lay the platform for future interac-tions over resources. For example, an extroverted dog mayset the stage for subsequent encounters with an introverteddog over equally valued resources. Some dogs may beunable to interpret the intentions of unfamiliar dogs whenthey approach conspecifics; they may be less concernedwith resources than with the need to obviate a perceivedthreat. Clinical experience suggests that some dogs willbehave in an aggressive manner toward any unfamiliar dog,in any setting, at considerable distances (Debbie Calnon,personal communication). For these dogs, it is very difficultto identify the value of a resource because the most likelyprimary motivation appears to be fear or anxiety. Thisprompts us to ask whether access to self-defense mecha-nisms (and actions taken to reduce the perceived risk of harm to self) is the resource these dogs value.Scientists generally base their measurements of socialhierarchies on who displaces whom from food and, lessoften, on who initiates contact with whom. However, it isimportant to ask whether the order that predicts displace-ment and appeasement is sometimes based on relative valueof resources and sometimes on fear. Regardless, the ques-tion is whether such social order among dogs can include 106 Journal of Veterinary Behavior, Vol 7, No 2, March/April 2012  humans and whether perceived breaches of order mayexplain how humans occasionally get bitten. It is possiblethat inconsistency on the part of humans can createbehavioral conflict in nearby dogs and the resultant frus-tration can trigger aggression. Dogs that bite humans areusually, but not always, thought to bite because of fear andanxiety (McGreevy and Calnon, 2010). Of course, all non-biting dogs are not necessarily free of fear or anxiety solelybecause they are sure of their social status. Nevertheless,care is warranted in human activities that may amount toethologically relevant social threats to dogs.Conflicts between dogs living in the same household aremost often between members of the same sex, and moreoften involve females than males (Sherman et al., 1996;Wrubel et al., 2011). That said, the triggers for these ag-gressive encounters are generally reported by dog ownerswho are untrained in making behavioral observations.Thus, it is difficult to identify why these conflicts occurand why they are more prevalent between members of thesame sex than between members of the opposite sex.Free-ranging dogs living in groups are reported to show alinear hierarchy, but although there are differences in fre-quency of agonistic interactions between males and fe-males, there is no clear indication whether there is aseparate hierarchy for each sex (Pal et al. 1998). Scott and Fuller (1965) found that when male and female puppiescontested a resource, males tended to win. They postulatedthat this was because males were typically larger. However,between sexes, size had no effect on the outcome of con-tests in female–female pairs, and only a weak effect inmale–male pairs. Scott and Fuller (1965) concluded that arelationship tends to reflect the differential capacities of the 2 individuals involved. Thus, dogs of different sextend to have more defined relationships, with one membertypically playing the dominant role and the other playingthe subordinate, whereas dogs of the same sex tend tohave relationships that are less well-defined, with dominantand subordinate roles switching readily. The latter relation-ship is more likely to trigger aggressive behavior generatedby conflict. The relevance of canine social behavior  Moehlman (1987) reminds us that the regulation of social structure and behavior in wild canids reflects charac-teristics of the canid (size, weight, and sex), the group(group size, territory, and reproductive strategies), andaccess to food (temporal and spatial distribution of prey).Domestication has changed many of these variables beyondrecognition, and perhaps most of all in the supply of resources, especially food.Homologous behavioral mechanisms can be identifiedbetween wolves and dogs, but the best model for describingsocial relationships among domesticated dogs reared in ahome environment derives from that environment ratherthan any wild canid social structure (Wright, 2004). Much of the work on cognition in dogs has focused on testing pu-tativeeffectsofdomesticationofpetdogsandcomparingtheresults with captive, usually hand-reared wolves. Wolves inthese populations do not respond to human cues aboutlocation of items in the same way that dogs do, leading tothe conclusion that ‘‘pointing’’ or ‘‘showing’’ are behaviorsdeveloped because of close contact with humans, possiblybecause of domestication (Miklosi, 2007).The ability of dogs to gain access to particular resources,retain their own resources, and displace other dogs fromresources is a critical element of social order. Dogs arelimited to burying prized objects, but humans can stashresources in pockets, boxes, and cupboards that only theycan access. Dogs do not feed adult conspecifics nor, for thatmatter, do they dictate when they take exercise. A dog’sbehavior can be manipulated by identifying resourcesvalued by the individual dog. Resources such as food andexercise can be used by humans to encourage and discour-age particular canine behaviors, illustrating one distinctdifference between intra- and interspecific social relation-ships. It follows that resource supply, resource guarding,and resource-related frustration (on the part of dogs) canprove problematic in some dog–human dyads.Most operant conditioning uses learning theory to modifydog behavior. We control access to the resources and, usingthem,cantrainallthebehaviorsweregardasdesirable.Thisissomethingotherdogsdonotappeartodoaseffectivelyaswedo. Thus, again, we need to be cautious because it may bewrongtoassumethatdogswanttocontrolotherdogsthroughaccess to resources. From ethological descriptors, a socialanimal is accorded rank through its ability to gain access tospecific resources. However, we emphasize that it does notfollowthattheanimalismotivatedtotakecontrolofresourcestoattainrank.Inotherwords,theanimalisnotmotivatedbyadesire to be dominant for the sake of attaining rank per se. The role of social learning Social learning occurs when an individual learns byobservation of another individual (Ligout, 2010). In somespecies, such as domestic chickens, the social status of the demonstrator has a strong influence on the perceivedvalue of the information it imparts (Nicol and Pope,1999). Social learning is an important aspect of the dog’ssocial behavior (Horowitz, 2009a); thus, we should con- sider how canine ethology informs the way in which weapply learning theory.Cognitive tests can include truly novel components thatrequire learning during the test, including situations inwhich dogs learn from watching other dogs successfullyperform and be rewarded for performing a novel task (Range et al., 2009). It has been shown that the pups of trained drug-detection bitches learned to pay attention totarget odors from watching their mothers (Slabbert andRasa, 1997). In another study, observer dogs were able toadjust their search behavior for hidden food depending on McGreevy et al Overview of the dog–human dyad 107
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