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44 / / Veterinary Focus / / Vol 20 No 1 / / 2010

IntroductionMost people have no difficulty in identifyingovert aggression and fear, but the interactionbetween these is less frequently recognized. Fearis an emotional reaction associated with thepresence of potentially harmful stimuli (by contrast, anxiety arises from the anticipation of such events, although the terms will be usedinterchangeably here) and is typically expressed in

one of three obvious ways. When an animal judgesthat the most appropriate way to deal with suchthreats is to avoid them ( i.e. take flight) then thecommonly recognized fear response is elicited. If however, it decides to keep still, ("freeze") then theinvolvement of fear is perhaps less obvious, andif it attempts to eliminate the stimulus from itsproximity ( i.e. engage the "fight" response), thedog's behavior may result in inappropriate and

potentially harmful interactions initiated by people, who frequently misunderstand this assome sort of dominance gesture. A dogs initialchoice of action may change in both the short term(i.e. there may be a switch in behavior) or longer term( i.e. the dog may use a different initial strategy in future similar contexts) depending on what seemsto happen next from the dogs perspective ( e.g. thethreat continues, intensifies or the dispute is resolv-ed). Thus, far from being an instinct ive impulse,aggress ion is often a carefully (but quickly)evaluated strategy aimed at resolving a dilemma

for the animal involving some perceived threat.

Daniel Mills, BVSc PhDCBiol FIBiol FHEA CCABDip ECVBM-CA MRCVSEur opean & RCVS Recogni zed Speciali st in Veterin ary Behavi oural Medicine, Dept of Biol ogical Sciences, Uni versity of Lincoln, UK

Professor Mills graduated from Bristol Veterinary School in1990 and was the first individual to be recognized by theRCVS as a specialist in veterinary behavioral medicine; hewas awarded his Chair at the University of Lincoln in 2004.His main area of research interest concerns animal cogn-ition and emotional regulation. He is the program leader of

the University's MSc in Clinical Animal Behavior.

Helen Zulch,BVSc(Hons) MRCVS

Ani mal Behaviour, Cognition and Welf are Group, Dept of

Biol ogical Sciences, Uni versity of Lincoln, UK

Dr. Zulch graduated from the veterinary faculty of theUniversity of Pretoria in 1992. The majority of her careerhas been spent lecturing, first physiology and then AnimalBehavior. She joined Lincoln University at the beginningof 2008 where she consults in the Behavior Referral Clinicas well as lecturing on under-graduate and post graduateprograms.

Appreciating the role of fearand anxiety in aggressive

behavior by dogs

KEY POINTSDogs can respond to a potentially harmful stimulusby flight, freeze or fight strategies

It is essential to appreciate the factors thatcontribute towards fear inducement

Dogs use a complex of body language that has to betaken together to understand their preferences inconflict situations

There is no direct evidence of dominance as amotivating factor for aggression in dogs

Published in IVIS with the permission of the editor Close window to return to IVIS


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Vol 20 No 1 / / 2010 / / Veterinary Focus / / 45

This is not to say that all aggressive behavior ismotivated by fear. Indeed, aggression is notconsistently associated with any single emotionalstate, but may be used to label any behavior that isperceived to actually or potentially cause harm toanother. This means that behaviors in which harmis incidental ( e.g. if a dog should nip as part of play) may be described as a form of aggression(play aggression); as may behaviors associated with the acquisition of food (predatory aggression).However, these responses are motivationally quitedistinct and there is an increasing tendency to usethe terms play and predation to describe thesebehaviors (1), avoiding the term aggression as thismay give rise to confused thinking about theircause and management. This clarification may beone of the first things to address when presented with a case in which someone or something hasbeen harmed. It is suggested that the termaffective aggression be used to refer to behaviorassociated with the presence of negative emot-ional arousal, such as a state of fear. Howevernote that, while it is important to recognize thecircumstances that might give rise to fear (Figure1) , it is unwise to consider that any emotionunderlying an aggressive episode is fixed ornecessarily consistent; for example if a dog isdenied access to a resource by an individual whois perceived as a threatening competitor, (whichmay be the owner), then the aggressive responsemay include elements of both fear and frustration.

Veterinarians need a greater appreciation of therisk factors for the involvement of fear in aggres-sion, since greater provocation will furthercompromise the animals welfare and potentially increase the risk to others. To this end there aretwo important points to consider in the recog-nition of fear-related aggression:

What circumstances give rise to a fear response? Why is aggression chosen as part of the strategy

involving fear?

Ci rcum st an ces givi ng ri se to fear i n dogs It is worth highlighting that, due to interactionsbetween genetic and experiential factors, someindividuals are more sensitive to fear than others,regardless of their experience. Both breeding and

early experience may therefore have important

roles to play in the risk of a fear response beingexpressed (all other factors being equal) by a givenindividual in certain circumstances, but thissection will focus upon the specific factors whichpredispose an animal to show a fear response in agiven situation.

Many specific fears are learned as a result of anaversive experience, for example the fear of a veterinarian who has handled the animal roughly,especially if it was in pain, and the relevance of this in any given case can often be identified by acareful history. However there is also a range of factors that (unless there is specific training tothe contrary) can have an intrinsic threateningquality. These can help a dog to avoid harm by providing general rules that aid the judgementof potential risk and how to respond. These areparticularly important when the animal lacksclear signals about its safety and they can serveas triggers for a fear response and possibleaggression as a consequence. These factors can bebroadly divided into stimulus characteristics andenvironmental features, whose significance in agiven case can be evaluated and used to helpinform treatment priorities (Table 1) .

Sti mu lu s char acteristics Trajectory. The direction of movement of anindividual towards a dog can have a marked effect

on how that individual is perceived. Direct appr-

Figure 1. The looming of this owner over their dog is a typical trigger fora fear aggressive response, even though the owner thinks theyare being friendly trying to pat it.



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oaches are generally perceived as more threat-ening than indirect approaches and so are morelikely to evoke a fear response.Velocity. All other things being equal, rapidmovement is more likely to be perceived asthreatening than slow movementAcceleration. A sudden increase in the speed of movement is often a sign of impending danger,and so abrupt movements around a dog may beperceived as potentially threatening.Size. Bigger objects are generally associated witha greater capacity to cause harm and so are morelikely to evoke a fear response than smaller ones.Direction. In many species vertical movementacross the retinal field is generally seen as moreintimidating than horizontal movement. Why thisshould be so is unclear, but this is not limited to theperception of whole body movements; moving ahand vertically in front of a dog is often more likely to elicit a fear response than moving the handhorizontally at the same speed.Looming. Many species find the act of beingleaned over by another as intimidating (2). Thusstanding half a meter away from a dog is not the

same as doing this with your hand outstretchedover it at a similar distance.

Environm ent al cues (adapted from Archer ( 3)) Novelty. An unfamiliar environment or unexp-ected event is more likely to elicit a fear responseas the animal does not have the necessary inform-ation about its security (4).Allocentric spatial thresholds. Allocentric space( i.e. the location of objects relative to one anotheror some arbitrary point) may be used to define thelocation of important geographical boundariesto an individual, such as the limits of a territory.Crossing of these boundaries by an unfamiliarindividual may be perceived as potentially threat-ening (5). This area contains important resourcesfor an individual and so its invasion could signaltheir potential loss, and so many territorial defensebehaviors are associated with self-protection andcan involve a fear component. The crossing of theterritorial boundary associated with the home isperhaps the most obvious allocentric threshold which can elicit a defensive response. However,in some cases, dogs may define more arbitrary

The dog is on its bed in the livingroom with a toy next to the bed. Atoddler approaches the dog, lifts thetoy and reaches towards the dog toreturn the toy to the dog. The dogsnaps at the child (6).

Older dog suffering from arthritis haspreviously traveled with a young boist-erous dog in the back of a car. Olderdog has now started growling at theyounger dog when he tries to climbinto the car.

Young toy breed dog has begun lung-ing and barking at approaching dogswhen out walking. Has previously beenexposed to puppy classes allowinguncontrolled free play sessions withmultiple dogs.

Personal space invaded. Possessionthreatened. Looming action of child.Movement of child and its body partsmay be erratic and so include bouts of acceleration.

Pain associated with the youngstersprevious actions in the car. Invasion of personal space.

Pain or fear associated with previousinteraction with other dogs at puppyclass. Owner may have attempted tocorrect what they perceive as mis-behavior, i .e. owners behavior is alsothreatening to the dog.

Control access by children to dog when heis resting. Discourage child from pickingup dog toys. Desensitise dog to approachesto bed. Desensitise dog to looming actionsand accelerations in its proximity. Instituteexchange programs for all those items whichthe dog may perceive to be of value so thathuman possession of the items becomespositive.

Control pain. Restrain young dog when inthe back of the car. Counter condition theolder dog to the presence of the young dogin the car.

Stop punishment and threatening actionsof owner towards their dog. Prevent theyoung dog from practicing the behavior.Desensitise and counter condition the dogto other dogs in all situations where theymay be encountered.

Tabl e 1.

Examples of aggressive behavior problems involving stimuli which may elicit fear

Scenario Possible threat elementsperceived by the dogAdvice to client



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Avoidance of conflict through yielding /withdrawal

Appeasement (aiming to re-establishnon-confrontational social contact)

Encourage another to withdraw(which may still be motivated by fear)

Approach / avoidance or other form of emotional conflict. This may not signala desire for immediate action butdemonstrates a level of discomfort withthe current situation which may indicatean increased risk for fear motivatedaggression.

Avert gaze or turn head away Curve body away and/or move away Slow downand/or curved approach Stop Tail tuck / arch back Lower body / lower neck Stiffen body Weight over hindquarters Piloerection Molars exposed with wide open mouth Retract lips to elongatecommisure Retract lips to expose incisors in smile Narrow eyes / blink Foldears back Lie down in lateral recumbence Raise hind leg whilst in lateralrecumbence Raise head with gaze averted

Slow down and/ or curved approach Stop Wagging tail Tail tuck / arch back Lower body Piloerection Avert gaze Lie down lateral or dorsal recumbence

Raise hind leg whilst in lateral recumbence Paw lift Yawning / retract lips / lipli ck Narrow eyes / blink Fold ears back Lower neck Reach up towardsmouth area of other individual possibly with licking motions

Direct rapid approach Direct steady tense deliberate approach Weight overforequarters Tail raised above normal relaxed carriage for individual Waggingtail / still , stiff tail Ears pricked / lateral / flattened against skull Lip commisurepulled forwards Incisors / canines exposed with wrinkled muzzle skin Mydriasis Direct stare / widened eyes with tension of surrounding musculature Neck archedand head raised / muscle tension Stillness Lunge / snap / bite

Lip licking / yawning Piloerection Shaking (as if to rid coat of water) Otherdisplacement activities such as sniffing the ground

Tabl e 2.

Interpreting the dogs body language. These interpretations are putative as few have beenrigorously examined in a scienti fic manner. Postures demonstrated in any given context varyaccording to the individual and its previous experience

Putative motivation for the action Body Language exhibited

territories, such as the space around the car thatthey are within when it is parked, and respond tothe potential invasion of this space in a similar way.

Egocentric spatial thresholds. Not all of the spacein which an individual exists is defined by itsphysical location; egocentric space is defined by reference to its location relative to the individual(2). As humans we are familiar with the idea of our personal space, a certain distance that we wish to keep from others to maintain our comfortin normal circumstances. If this space is invadedthen we will often respond (if possible) in some way, such as backing off. For dogs there are at leasttwo important egocentric spatial thresholdsthat are associated with activation of the fearneurocircuitry: the invasion of the dogs personal

space and invasion of its body surface e.g. touch.

The personal space of a dog appears to be typically between 1.5 and 2 meters in an open situation, butit may vary depending on the characteristics of theenvironment. Just as we may tolerate people closerto us in a crowded train carriage, so too may a dogreduce its personal space in an equivalent situation.However, in both there is still a minimum accept-able distance, defined according to the region of the body concerned. We may tolerate greaterproximity of the body trunk than the face, forexample. In situations such as this it may be part-icularly important for the individuals to com-municate their non-threatening intent in order toavoid inadvertent elicitation of a fear response.

Th e deci si on t o express aggressi on as part of a fear response As mentioned above, an animal may evoke one

of three strategies to deal with a potential threat:

APPRECIATING THE ROLE OF FEAR AND ANXIETY IN AGGRESSIVE BEHAVIOR BY DOGS



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flight, freezing or fighting. Many animals may freeze to allow the threat to pass, but this can failas a strategy because the owner perceives thisbehavior as stubbornness and responds in athreatening way to the dog, and so escalates theperceived threat. If freezing does not succeed,then the animal has little choice other than to try to withdraw itself or get the perceived threat to withdraw. Withdrawal may not be possible ( e.g. if the dog is cornered or restrained in some way,such as with a lead), and so the dog then has nosensible choice other than to try to get the threatto withdraw. This is done using a sequence of conflict-related gestures, which may ultimately involve overtly aggressive behavior if more subtlegestures are ineffective at resolving the situation.In other situations it may be theoretically possiblefor the animal to flee, but it is strongly motivatednot to do so. This might be because:

It wants to protect a resource that it valueshighly and/or which it cannot easily take withit, for example a bitch protecting her puppies

It anticipates that the other individual will give way, for example because it is smaller, weakerand/or has yielded in the past

It has learned that other strategies do not work, e.g. when it freezes, the owner continues to tell it off

It would be painful to do so e.g. concurrent hipdysplasia

Once again, the response of the individual whohas provoked the response in the dog is critical indetermining what happens next. Do they escalatethe confrontation or not? Escalation may occurbecause one or more of the innate triggers of aggression is presented (such as approaching andleaning over the dog) or because a direct threat ismade ( e.g. the owner gets angry). Ultimately thismay lead to an aggressive display by the dog (7),but it is important to appreciate that this will beunderpinned by an element of fear, because theanimal feels threatened.

Signal in g to avoid overt aggression An aggressive display should be viewed as a failureto understand the animals needs at a given time,since dogs have a well-developed communicationsystem designed to minimize the risk of escalationand avoid physical conflict in the face of a

potential threat (Table 2) . This is because overt

physical attack is a potentially risky strategy, which, even if successful, may lead to injury ordisruption of the social group to such an extentthat the long term biological fitness of antagonists will be compromised. Nature does not favor thetendency to fight unless the situation is perceivedas serious. When there is a potential conflict of interests, dogs will typically communicate atleast two distinct messages to avoid unnecessary escalation:

Their preferred level of engagement in theconflict ( i.e. their desire to yield versus opposethe other)

Their level of hostility (intention to inflict harmor not) to resolve the dispute

Yielding is generally shown through body posturesconsistent with withdrawal or inconsistent withengagement, such as a low, crouched posture withears back and tail tucked or the exposure of thebelly and aversion of eye gaze, while opposition isexhibited by a more forward posture and action.These are frequently described as submissive orfearful versus dominant or confident postures, butnote that they relate to preference for engage-ment in a given situation rather than an exhibitionof general social status, i.e. they are context specificalthough they may be shaped by previous experience.

Hostility is evident from an increase in arousaltogether with more specific warning signs such asthe fixing of gaze, baring of the teeth, vocalizationand snapping. By contrast, appeasement, whichsignals a non-hostile intent and aims to reducehostility in others, can be expressed through arange of gestures such as yawning, increasedblinking, slow movement, reduced ocular apert-ure, and nose licking.

The expression of yielding and hostility is perhapsmost readily interpreted as a fear-biting scenario,but it is important to recognize that even an animal who is willing to actively oppose another may befearful of the consequences (8). For example it may be willing to protect a valued resource but may stillbe concerned about the outcome. Therefore thetendency to interpret the posture of engagement asa sign of confidence is erroneous. This may explainthe finding by Guy (9) that supposedly dominantly

aggressive dogs are generally anxious and not



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1. De Keuster T, J ung H. Aggression toward familiar people and animals.In: Horwitz DF & Mills DS (eds). BSAVA M anu al of Cani ne and Felin e Behavioural Medicine (2nd edn). 2009; pp. 182-210.

2. Graziano MFA, Cooke DF. Parieto-frontal interactions, personal space,and defensive behavior. Neuropsychologia 2006; 44 : 845-859.

3. Archer J . The organization of aggression and fear in vertebrates.In: Bateson PPG, Klopfer PH (eds) Perspecti ves in Ethol ogy , Vol. 2,Plenum Press , New York 1976; pp. 231-298.

4. Marler P. On animal aggression: the roles of strangeness andfamiliarity. Am erican Psychologist 1976; 31 : 239-246.

5. Hediger H. (Sircom G, transl.) The psychology and behaviour of

animals in zoos and circuses. Butterworth, New York 1963.

6. Reisner IR, Shofer F, Nance M. Behavioral assessment of child-directedcanine aggression. Inju ry Preventi on 2007; 13 : 348-351.

7. Herron M, Shofer FS, Reisner IR. Survey of the use and outcome of confrontational and non-confrontational training methods in client-owned dogs showing undesirable behaviors. Applied Ani mal Behaviour Science 2009; 117 : 47-54.

8. Fatj J, Feddersen-Petersen D, Lus J , et al. Ambivalent signals duringagonistic interactions in a captive wolf pack. Appl A ni m Behav Scien 2007; 105 : 274-283.

9. Guy NC, Luescher UA, Dohoo SE, et al. A case series of biting dogs:characteristics of the dogs, their behaviour, and their victims. Appl An im Behav Scien 2001; 74 : 43-57.

R EFERENCES

confident as might be predicted if dominance wasreally underlying the behavior. Indeed, to theauthors knowledge, there is no direct evidence of dominance as a motivating factor for aggression indogs, although it is often implied by observers.

Several other important implications follow fromthis evaluation of the signaling of dogs. First, if adog exhibits signs of appeasement and these arenot acknowledged, then it may either show moreintense signs of appeasement or decide thathostility is necessary since appeasement doesnot seem to work. Appropriate acknowledgementinvolves disengaging and eliminating any gest-ures which could be perceived as potentially threatening. Unfortunately many owners mistakeappeasement gestures for a guilty dog who knowshe has done wrong (Figure 2) , and this can resultin further threatening gestures from the owner,leading the animal to reject attempts at reconcil-iation and so resort to hostility instead. Unfort-unately, the dog may learn from such encountersthat appeasement is not a useful strategy andtherefore only offer hostility when afraid in thefuture. A similar account could be described inrelation to failure to respond appropriately to yielding (as opposed to active appeasement)behavior. In either case the aggression that resultsis both normal and a response to continued threatand so rightly considered a form of fear-relatedaggression. Of particular importance to theeffective and humane management of these casesis recognition that fear may feature within a dogopposing another in any competitive situation.Treatments which might potentially escalate the

problem ( e.g. those based on punitive or potent-ially threatening assertive interaction, rather thanconsistent sensitive recognition of the animalsneeds) should be rejected.

ConclusionFear is involved in the expression of aggressionfar more frequently than is perhaps generally recog-nized. It is essential that everyone who interacts with dogs recognize both the stimuli which may be perceived as threatening to dogs as well as themeans dogs use to signal their willingness toengage in different strategies in social situations.Only then can the risk of aggression and biting bereduced effectively in the long term.

Figure 2.An owner may interpret appeasement behavior as a guilty

look; note the dogs crouched body stance, tensed neck,lowered head, narrowed eyes, folded ears and tucked tail.

APPRECIATING THE ROLE OF FEAR AND ANXIETY IN AGGRESSIVE BEHAVIOR BY DOGS


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