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Appreciating the role of fear and anxiety in aggressive behavior by dogs

Daniel Mills, BVSc PhD CBiol FIBiol FHEA CCAB Dip ECVBM-CA MRCVS
European & RCVS Recognized Specialist in Veterinary Behavioural Medicine, Dept of Biological Sciences, University of Lincoln, UK
Professor Mills graduated from Bristol Veterinary School in 1990 and was the first individual to be recognized by the RCVS as a specialist in veterinary behavioral medicine; he was awarded his Chair at the University of Lincoln in 2004. His main area of research interest concerns animal cognition and emotional regulation. He is the program leader of the University's MSc in Clinical Animal Behavior.

Helen Zulch,
BVSc(Hons) MRCVS
Animal Behaviour, Cognition and Welfare Group, Dept of Biological Sciences, University of Lincoln, UK

Dr. Zulch graduated from the veterinary faculty of the University of Pretoria in 1992. The majority of her career has been spent lecturing, first physiology and then Animal Behavior. She joined Lincoln University at the beginning of 2008 where she consults in the Behavior Referral Clinic as well as lecturing on under-graduate and post graduate programs.

Introduction
Most people have no difficulty in identifying overt aggression and fear, but the interaction between these is less frequently recognized. Fear is an emotional reaction associated with the presence of potentially harmful stimuli (by contrast, anxiety arises from the anticipation of such events, although the terms will be used interchangeably here) and is typically expressed in

KEY POINTS
Dogs can respond to a potentially harmful stimulus by flight, freeze or fight strategies It is essential to appreciate the factors that contribute towards fear inducement Dogs use a complex of body language that has to be taken together to understand their preferences in conflict situations There is no direct evidence of dominance as a motivating factor for aggression in dogs

one of three obvious ways. When an animal judges that the most appropriate way to deal with such threats is to avoid them (i.e. take flight) then the commonly recognized fear response is elicited. If however, it decides to keep still, ("freeze") then the involvement of fear is perhaps less obvious, and if it attempts to eliminate the stimulus from its proximity (i.e. engage the "fight" response), the dog's behavior may result in inappropriate and potentially harmful interactions initiated by people, who frequently misunderstand this as some sort of dominance gesture. A dogs initial choice 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 seems to happen next from the dogs perspective (e.g. the threat continues, intensifies or the dispute is resolved). Thus, far from being an instinctive impulse, aggression is often a carefully (but quickly) evaluated strategy aimed at resolving a dilemma for the animal involving some perceived threat.

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This is not to say that all aggressive behavior is motivated by fear. Indeed, aggression is not consistently associated with any single emotional state, but may be used to label any behavior that is perceived to actually or potentially cause harm to another. This means that behaviors in which harm is 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 quite distinct and there is an increasing tendency to use the terms play and predation to describe these behaviors (1), avoiding the term aggression as this may give rise to confused thinking about their cause and management. This clarification may be one of the first things to address when presented with a case in which someone or something has been harmed. It is suggested that the term affective aggression be used to refer to behavior associated with the presence of negative emotional arousal, such as a state of fear. However note that, while it is important to recognize the circumstances that might give rise to fear (Figure 1), it is unwise to consider that any emotion underlying an aggressive episode is fixed or necessarily consistent; for example if a dog is denied access to a resource by an individual who is perceived as a threatening competitor, (which may be the owner), then the aggressive response may include elements of both fear and frustration. Veterinarians need a greater appreciation of the risk factors for the involvement of fear in aggression, since greater provocation will further compromise the animals welfare and potentially increase the risk to others. To this end there are two important points to consider in the recognition of fear-related aggression: What circumstances give rise to a fear response? Why is aggression chosen as part of the strategy involving fear?

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

roles to play in the risk of a fear response being expressed (all other factors being equal) by a given individual in certain circumstances, but this section will focus upon the specific factors which predispose an animal to show a fear response in a given situation. Many specific fears are learned as a result of an aversive 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 a careful history. However there is also a range of factors that (unless there is specific training to the contrary) can have an intrinsic threatening quality. These can help a dog to avoid harm by providing general rules that aid the judgement of potential risk and how to respond. These are particularly important when the animal lacks clear signals about its safety and they can serve as triggers for a fear response and possible aggression as a consequence. These factors can be broadly divided into stimulus characteristics and environmental features, whose significance in a given case can be evaluated and used to help inform treatment priorities (Table 1).

Circumstances giving rise to fear in dogs

It is worth highlighting that, due to interactions between genetic and experiential factors, some individuals are more sensitive to fear than others, regardless of their experience. Both breeding and early experience may therefore have important

Stimulus characteristics
Trajectory. The direction of movement of an individual towards a dog can have a marked effect on how that individual is perceived. Direct appr-

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oaches are generally perceived as more threatening than indirect approaches and so are more likely to evoke a fear response. Velocity. All other things being equal, rapid movement is more likely to be perceived as threatening than slow movement Acceleration. A sudden increase in the speed of movement is often a sign of impending danger, and so abrupt movements around a dog may be perceived as potentially threatening. Size. Bigger objects are generally associated with a greater capacity to cause harm and so are more likely to evoke a fear response than smaller ones. Direction. In many species vertical movement across the retinal field is generally seen as more intimidating than horizontal movement. Why this should be so is unclear, but this is not limited to the perception of whole body movements; moving a hand vertically in front of a dog is often more likely to elicit a fear response than moving the hand horizontally at the same speed. Looming. Many species find the act of being leaned over by another as intimidating (2). Thus standing half a meter away from a dog is not the

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

Environmental cues (adapted from Archer (3))

Novelty. An unfamiliar environment or unexpected event is more likely to elicit a fear response as the animal does not have the necessary information about its security (4). Allocentric spatial thresholds. Allocentric space (i.e. the location of objects relative to one another or some arbitrary point) may be used to define the location of important geographical boundaries to an individual, such as the limits of a territory. Crossing of these boundaries by an unfamiliar individual may be perceived as potentially threatening (5). This area contains important resources for an individual and so its invasion could signal their potential loss, and so many territorial defense behaviors are associated with self-protection and can involve a fear component. The crossing of the territorial boundary associated with the home is perhaps the most obvious allocentric threshold which can elicit a defensive response. However, in some cases, dogs may define more arbitrary

Table 1. Examples of aggressive behavior problems involving stimuli which may elicit fear
Scenario The dog is on its bed in the living room with a toy next to the bed. A toddler approaches the dog, lifts the toy and reaches towards the dog to return the toy to the dog. The dog snaps at the child (6). Possible threat elements perceived by the dog Personal space invaded. Possession threatened. Looming action of child. Movement of child and its body parts may be erratic and so include bouts of acceleration. Advice to client Control access by children to dog when he is resting. Discourage child from picking up dog toys. Desensitise dog to approaches to bed. Desensitise dog to looming actions and accelerations in its proximity. Institute exchange programs for all those items which the dog may perceive to be of value so that human possession of the items becomes positive. Control pain. Restrain young dog when in the back of the car. Counter condition the older dog to the presence of the young dog in the car.

Older dog suffering from arthritis has previously traveled with a young boisterous dog in the back of a car. Older dog has now started growling at the younger dog when he tries to climb into the car. Young toy breed dog has begun lunging and barking at approaching dogs when out walking. Has previously been exposed to puppy classes allowing uncontrolled free play sessions with multiple dogs.

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

Pain or fear associated with previous interaction with other dogs at puppy class. Owner may have attempted to correct what they perceive as misbehavior, i.e. owners behavior is also threatening to the dog.

Stop punishment and threatening actions of owner towards their dog. Prevent the young dog from practicing the behavior. Desensitise and counter condition the dog to other dogs in all situations where they may be encountered.

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

Table 2. Interpreting the dogs body language. These interpretations are putative as few have been rigorously examined in a scientific manner. Postures demonstrated in any given context vary according to the individual and its previous experience
Putative motivation for the action Avoidance of conflict through yielding / withdrawal Body Language exhibited Avert gaze or turn head away Curve body away and/or move away Slow down and/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 elongate commisure Retract lips to expose incisors in smile Narrow eyes / blink Fold ears back Lie down in lateral recumbence Raise hind leg whilst in lateral recumbence 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 / lip lick Narrow eyes / blink Fold ears back Lower neck Reach up towards mouth area of other individual possibly with licking motions Direct rapid approach Direct steady tense deliberate approach Weight over forequarters Tail raised above normal relaxed carriage for individual Wagging tail / still, stiff tail Ears pricked / lateral / flattened against skull Lip commisure pulled forwards Incisors / canines exposed with wrinkled muzzle skin Mydriasis Direct stare / widened eyes with tension of surrounding musculature Neck arched and head raised / muscle tension Stillness Lunge / snap / bite Lip licking / yawning Piloerection Shaking (as if to rid coat of water) Other displacement activities such as sniffing the ground

Appeasement (aiming to re-establish non-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 signal a desire for immediate action but demonstrates a level of discomfort with the current situation which may indicate an increased risk for fear motivated aggression.

territories, such as the space around the car that they are within when it is parked, and respond to the potential invasion of this space in a similar way. Egocentric spatial thresholds. Not all of the space in which an individual exists is defined by its physical 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 comfort in normal circumstances. If this space is invaded then we will often respond (if possible) in some way, such as backing off. For dogs there are at least two important egocentric spatial thresholds that are associated with activation of the fear neurocircuitry: 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, but it may vary depending on the characteristics of the environment. Just as we may tolerate people closer to us in a crowded train carriage, so too may a dog reduce its personal space in an equivalent situation. However, in both there is still a minimum acceptable distance, defined according to the region of the body concerned. We may tolerate greater proximity of the body trunk than the face, for example. In situations such as this it may be particularly important for the individuals to communicate their non-threatening intent in order to avoid inadvertent elicitation of a fear response.

The decision to express aggression as part of a fear response

As mentioned above, an animal may evoke one of three strategies to deal with a potential threat:

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flight, freezing or fighting. Many animals may freeze to allow the threat to pass, but this can fail as a strategy because the owner perceives this behavior as stubbornness and responds in a threatening way to the dog, and so escalates the perceived 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 no sensible choice other than to try to get the threat to withdraw. This is done using a sequence of conflict-related gestures, which may ultimately involve overtly aggressive behavior if more subtle gestures are ineffective at resolving the situation. In other situations it may be theoretically possible for the animal to flee, but it is strongly motivated not to do so. This might be because: It wants to protect a resource that it values highly and/or which it cannot easily take with it, for example a bitch protecting her puppies It anticipates that the other individual will give way, for example because it is smaller, weaker and/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 hip dysplasia Once again, the response of the individual who has provoked the response in the dog is critical in determining what happens next. Do they escalate the confrontation or not? Escalation may occur because one or more of the innate triggers of aggression is presented (such as approaching and leaning over the dog) or because a direct threat is made (e.g. the owner gets angry). Ultimately this may lead to an aggressive display by the dog (7), but it is important to appreciate that this will be underpinned by an element of fear, because the animal feels threatened.

physical attack is a potentially risky strategy, which, even if successful, may lead to injury or disruption of the social group to such an extent that the long term biological fitness of antagonists will be compromised. Nature does not favor the tendency to fight unless the situation is perceived as serious. When there is a potential conflict of interests, dogs will typically communicate at least two distinct messages to avoid unnecessary escalation: Their preferred level of engagement in the conflict (i.e. their desire to yield versus oppose the other) Their level of hostility (intention to inflict harm or not) to resolve the dispute Yielding is generally shown through body postures consistent with withdrawal or inconsistent with engagement, such as a low, crouched posture with ears back and tail tucked or the exposure of the belly and aversion of eye gaze, while opposition is exhibited by a more forward posture and action. These are frequently described as submissive or fearful versus dominant or confident postures, but note that they relate to preference for engagement in a given situation rather than an exhibition of general social status, i.e. they are context specific although they may be shaped by previous experience. Hostility is evident from an increase in arousal together with more specific warning signs such as the fixing of gaze, baring of the teeth, vocalization and snapping. By contrast, appeasement, which signals a non-hostile intent and aims to reduce hostility in others, can be expressed through a range of gestures such as yawning, increased blinking, slow movement, reduced ocular aperture, and nose licking. The expression of yielding and hostility is perhaps most 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 be fearful of the consequences (8). For example it may be willing to protect a valued resource but may still be concerned about the outcome. Therefore the tendency to interpret the posture of engagement as a sign of confidence is erroneous. This may explain the finding by Guy (9) that supposedly dominantly aggressive dogs are generally anxious and not

Signaling to avoid overt aggression

An aggressive display should be viewed as a failure to understand the animals needs at a given time, since dogs have a well-developed communication system designed to minimize the risk of escalation and avoid physical conflict in the face of a potential threat (Table 2). This is because overt

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

confident as might be predicted if dominance was really underlying the behavior. Indeed, to the authors knowledge, there is no direct evidence of dominance as a motivating factor for aggression in dogs, although it is often implied by observers. Several other important implications follow from this evaluation of the signaling of dogs. First, if a dog exhibits signs of appeasement and these are not acknowledged, then it may either show more intense signs of appeasement or decide that hostility is necessary since appeasement does not seem to work. Appropriate acknowledgement involves disengaging and eliminating any gestures which could be perceived as potentially threatening. Unfortunately many owners mistake appeasement gestures for a guilty dog who knows he has done wrong (Figure 2), and this can result in further threatening gestures from the owner, leading the animal to reject attempts at reconciliation and so resort to hostility instead. Unfortunately, the dog may learn from such encounters that appeasement is not a useful strategy and therefore only offer hostility when afraid in the future. A similar account could be described in relation to failure to respond appropriately to yielding (as opposed to active appeasement) behavior. In either case the aggression that results is both normal and a response to continued threat and so rightly considered a form of fear-related aggression. Of particular importance to the effective and humane management of these cases is recognition that fear may feature within a dog opposing another in any competitive situation. Treatments which might potentially escalate the

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.

problem (e.g. those based on punitive or potentially threatening assertive interaction, rather than consistent sensitive recognition of the animals needs) should be rejected.

Conclusion
Fear is involved in the expression of aggression far more frequently than is perhaps generally recognized. It is essential that everyone who interacts with dogs recognize both the stimuli which may be perceived as threatening to dogs as well as the means dogs use to signal their willingness to engage in different strategies in social situations. Only then can the risk of aggression and biting be reduced effectively in the long term.

REFERENCES
1. De Keuster T, Jung H. Aggression toward familiar people and animals. In: Horwitz DF & Mills DS (eds). BSAVA Manual of Canine and Feline 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) Perspectives in Ethology, Vol. 2, Plenum Press, New York 1976; pp. 231-298. 4. Marler P. On animal aggression: the roles of strangeness and familiarity. American 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-directed canine aggression. Injury Prevention 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 clientowned dogs showing undesirable behaviors. Applied Animal Behaviour Science 2009; 117: 47-54. 8. Fatj J, Feddersen-Petersen D, Lus J, et al. Ambivalent signals during agonistic interactions in a captive wolf pack. Appl Anim 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 Anim Behav Scien 2001; 74: 43-57.

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