Sunday 3 May 2015

Aggression in dogs

Dogs fulfil numerous roles within the human community. To early man, the main purpose for owning dogs is thought to have been their hunting prowess and the protection they conferred against other predators (Morris 2008). To date dogs continue to fulfil these roles  (Udell et al 2014), and for some they are  companions, confidants, and a member of the family (Overall 2013),  for others the dog is a work partner, an assistant, a status symbol, perhaps even a weapon (Morris 2008). These diverse, roles fulfilled by dogs, result in differing expectations, differing attitudes and differing husbandry, resulting with differing normative beliefs of aggression (Anderson et al 2003).

Aggression is defined as hostile behaviour, which is intended to harm (Davenport 1996; Gross et al 2004). Aggression in dogs includes: growling, snarling, snapping, biting, barking, or lunging (Abrantes 2005).

There are many different classifications of aggression within the literature and the definitions vary with each author, add on top the different classifications of aggressive behaviour in behavioural modification in dogs where some do not agree with each other, or they look at it from a different angle, or the labels change with each author. The intention is to select as much relevant information relating to aggression to ensure that most motivations are covered.

There are two types of aggression in mammalian species: predatory aggression (sometimes called quiet biting attack) and affective aggression. Predatory aggression can be deemed as an unemotional because behaviour is driven by food procurement at some level; inflicted on a different species; and is a self rewarding behaviour (Armony 2013). On the other hand affective aggression is driven by emotions and for the most part these are defensive behaviours, although if defensive behaviours are not working they can result in offensive behaviour. (Clutton-Brock et al 2013; Székely et al 2010).

Lorenz defines aggression as the "driving power,” an instinct toward the preservation of life, all mammals do not learn to be aggressive. It is in their nature. (Lorenz, K. 1963;2005).

Scott (1966) pointed out that:
“Aggression is a poor scientific term, and chiefly functions as a convenient handle to relate phenomena described in more objective terms to practical human problems. What we are really concerned with is agonistic behavior, a behavioral system composed of behavior patterns having the common function of adaptation to situations involving physical conflict between members of the same species. We cannot analyze fighting behavior without also studying the alternate behavior patterns of escape, threat, "freezing", defensive posture, dominance and subordination, etc” (page 683;Scott, 1966).

From an ethological point of view, aggression in dogs can be characterised as an intensive, emotional, expressive response oriented against the object of the dog's frustration. Aggression is a phylogenetic, pre-domestication, instinctive state of animals of self-preservation importance. Dogs are carnivorous animals and as such they exhibit various forms of aggression ; interspecific aggression is oriented against different animal species, which includes offensive and defensive elements. Its most frequent form is self-protective aggression (Kottferovi et al 2008; Ryan 2013). Predatory aggression is a part of feeding behaviour of carnivores, although domestication in dogs has resulted in relaxation of the predatory sequence, some dogs exhibit behaviour which is part of predatory behaviour, e.g. visual exploration, hunting small animals and occasionally humans. The stimuli that usually induce this behaviour include olfactory and visual (Udell et al 2014; Kottferovi et al 2008) . As behaviour is governed by rules that associate stimuli with responses and outcomes (Zhang et al 2013), treating predatory aggression is difficult, it is an instinctive behaviour, therefore good management is essential whilst behavioural modification is being commenced: use of leads, and muzzling if there is a risk of injury. Desensitization with counter-conditioning can be effective in some instances to change a dogs' perception of falsely identified prey. Satisfying the needs of the dog is paramount, I have used David Ryan’s ( 2013) two ball method successfully with dogs enjoy the pursuit and grab part of the predatory sequence, and I direct owners to read this which explains it simply http://www.dog-secrets.co.uk/how-do-i-stop-my-dog- chasing/ however owners need to be motivated and comply effectively for this to help.

Defence systems in the mammalian brain are aimed at making immediate responses to threatening stimuli; and a behavioural inhibition system responsible for the suppression of behaviour that could enhance danger, these conflicting systems work in concert and engage distinct hierarchic circuits depending on increasing demand for cognitive processing (Stein et al 2010). Defensive aggression is related to fear, pain or threat of punishment and includes defensive or submissive signals before or during the aggression (Overall 2013).

Territorial aggression:
Territoriality: is defined as behaviour by which an organism lays claim to an area and defends it against intruders, which is generally a fixed territory; personal territory on the other hand moves with the individual and can expand or contract depending on the circumstances. Territoriality is a basic behavioural system and is characteristic of all living organisms (Hall 1969,1990). Some breeds of dogs; and some individual dogs, regardless of breed are more territorial than others (Beaver 2009). Territorial behaviour usually appears as puppies mature into adolescence or adulthood, at one to three years of age (Beaver 2009; Overall 2013).

Territoriality behaviour can be a way to insure they have a safe place, because a dog with a territory can develop an inventory of reflex responses when perceived danger strikes, rather than having to think about the environment they are in (Székely et al 2010). So a dog with who is fearful might well defend a place he feels safe in.

Space requirements are influenced by the environment. One of the most fundamental parts of territoriality is proper spacing which protects against over exploitation of that part of the environment (Hall 1969;1990). So a dog that is displaying territorial aggression it could be because they are living in over crowded conditions, or that there is a high densitiy of dogs/humans/other animals living in their neighbourhood. Hediger (1965) inferred the need for proper spacing between individuals, were species specific, and environmental specific. Flight distance and critical distance are used when two difference species meet, where as personal distance and social distance can be observed during interaction between members of the same species (Hall 1969;1990). And for some dogs the mechanism of personal distance and social distance only applies to members of their immediate household, all other humans and animals are treated as a different species even if they have had effective socialisation (Hall 1969,1990; Coppinger et al 1996).

Hediger (1965) he also identified a variation in difference between species, some animals are contact species and some are non contact animals. Species like the Emperor Penguin huddle together and require physical contact with each other. Although dogs fall under the non contact species they begin their life in the contact phase, which is temporary, the dam will naturally reduce contact times even if man did not intervene. Some dogs will continue to seek out close contact with housemates other dogs will ensure regular spacing is adhered too (Hall 1969,1990; Hediger 1965). As dogs are deemed to be non contact animals they are likely to be more vulnerable to stresses of overcrowding.

How to help a dog who presents with territory aggression is he in over crowded conditions, are there lots of people and animals in the neighbourhood, if that is the case it is going to be more at looking at ways of ensuring that the dog has more space or alter the environment so that he has his own personal space that is not likely to be encroached upon by others, putting up double fences so their is dead space between his territory and passerbys. Desensitization and counter conditioning will help. Alter walks if possible going to wide open places, or places where there is less foot-fall, preventing the behaviour from occurring is the best way. It also ensures that trigger stacking is minimised

Protective aggression occurs as a result of territorial behaviour regarding their owners, handlers and the children of the family or other animals that they have developed social bonds with (McGrew 1983). Livestock Guardian breeds like the Anatolian, German Shepherd and Maremma’s dogs etc have a long history of being bred for their protective role. There is a behavioural distinction between protective aggression and territorial aggression, Instead of defending a geographical location, these dogs actually defend the space immediately around them, their personal space. These dogs are generally very attentive to the individual/s being protected, and consequently those individuals become included within this defended area resulting in the dog being equally protective anywhere it encounters a predator or a falsely identified predator, like the mother in law, or the friendly neighbour. (Mcgrew 1983). Protective behaviour does not occur in puppies but it can develop as early as 9 months old (Mcgrew 1983) or as late as 18 months old (Coppinger et al 1988).

Maternal aggression is a form of protective aggression, but it is stimulated by hormonal factors. At the end of pregnancy or Dioestrus, there is a sudden drop in progesterone and an increase in Prolactin and a reduction in serotonin levels (Dahl et al 2010). However hormones do not cause or inhibit behaviour by themselves, rather they affect the sensitivity of the neural pathways involved in protective aggression.

Bitches are unique because they are designed to be pregnant after every heat cycle, the whole period is a pre-programmed finite lifespan and is not subject to the regression that you can be observed in other mammals like humans, horses, cattle etc when they do not conceive (Razzaque et al 2008). So the unsuspecting owner two months after the heat cycle cannot understand how their lovely girl has turned in to an aggressive being. Or how their lovely girl not long after being spayed turns aggressive. So whether the bitch has just had a litter, or has just been spayed, or two months after heat cycle their is a likely hood that they can develop maternal aggression. The best thing is to prevent the dog from displaying aggression, leave them in peace, do not encroach, do not remove the very things they are protecting (in some circumstances removal of the things they are protecting can help for instance the dog is taken out for a walk, someone removed those items the dog does not have the visual stimuli to continue behaviour when they return. Remove as much stress as possible within the environment. This is a short term hormonal behaviour, what you don’t want the bitch to  do is to continually practice protective behaviour and consequently learn in the absence of the stimulating hormones protective behaviour because it works. If the bitch is displaying maternal aggression in the absence of pregnancy it might be worth discussing a suitable time to spay, this would usually be during Pro-oestrus, where the effects of spaying will have minimal, hormonal impact.

Paternal Aggression this is similar to maternal aggression however unrelated males and bitches can also display this aggression, protecting a young dog from others whether that is dogs or humans or other animals. This can be seen when a new puppy comes into the household and forms social bonds with a resident adult dog.

Possessive aggression develops when the dog appropriates some objects, for example a bone, food, a toy. Resource guarding is a normal behaviour if humans are constantly removing resources or not providing enough resources resource guarding is further enhanced. Hunting dogs like the Airdale Terrier are bred to protect kills from others, so are more likely to develop resource guarding behaviour. This behaviour can be seen in all ages from pups to adulthood (Beaver 2009; Overall 2013).

Social Aggression Social behaviour is driven by two antagonistic motivational incentives affiliation and competition. Competition theory was a fundamental part of Darwinian theory. Driven by their selfish gene, individuals seek to maximise their genetic contribution to the next generation, through affiliation and competing with others (Clutton-Brook et al 2013).

Competition requires aggression at some level. Lorenz believes that species develop a number of mechanisms for redirecting or inhibiting intraspecific aggression. Ritualized fighting in which no animal is really hurt which dissipates aggression, and submissive behaviour can block it. Dogs with their ability to kill easily, have developed rituals and inhibitions limiting and formalizing intraspecific aggression (Lorenz, K. 1963;2005). Competitive male displays are widespread in social animals and are used to attract breeding partners and to repel rivals. Visual; vocal ;and olfactory displays are often combined and frequently reflect the signallers hormonal status; condition; and physical strength.

Sex related aggression During development the brain is the target site for steroid hormones, during the neonatal period both males and females are exposed to variant amounts of testosterone, a female between two male neonates is going to be exposed to more testosterone than a female between two females (Trainor et al 2006). Exposing females to testicular hormones masculinises components of the central nervous system(CNS). Prenatal chemical castration or surgical castration of the male allows the development of a more female-like CNS. In mammals, the sexual differentiation of the CNS has a significant role in shaping sexual preference and other reproductive activities. In addition, it influences food intake and body weight, territorial marking and aggressive behaviour, learning strategies, and play behaviour (Birger et al 2003).

Testosterone can be deemed a pro-hormone, because it is a precursor to which when converted into 5-alpha-dihydrotestosterone (5α-DHT) acts on androgen receptors or when converted into estradiol by the enzyme aromatase, acts on oestrogen receptors There is overwhelming evidence that most of the effects of testosterone in mediating aggression occur after aromatization. For example, in rats testosterone induced aggression is concurrent with an elevated level of aromatization and nuclear oestrogenic receptor activity in the hypothalamic/preoptic area. Treatment with an aromatase inhibitor blocked this aggression and lowered nuclear activated oestrogen receptors Furthermore the intensity of aggressive behaviour was directly correlated with the aromatase activity in the posterior hypothalamus (Trainor et al 2006). Therefore we can surmise that the hormones do not cause or inhibit behaviour by themselves, rather they affect the sensitivity of the neural pathways involved in different behaviours. For instance testosterone sensitizes the responsiveness for stimuli which are related to aggression so they need less visual stimuli from a rival or from a threat which will start the aggressive motor programmes when testosterone levels are high. Furthermore testosterone strengthens the motor output so aggressive behaviour is performed at higher intensity (Jenson 2007). Prolactin and low levels of serotonin sensitizes the responsiveness for stimuli which are related to defence behaviour (Dahl et al 2010).

It has been identified that the interaction between low serotonin and high testosterone levels in the central nervous system has a significant effect on the neural mechanisms involved in the expression of aggressive behaviour. It seems that testosterone modulates serotonergic receptor activity in a way that directly affects aggression, fear and anxiety. Low serotonin exhibited high rates of aggression, high testosterone further augmented rates and intensity of aggression in subjects with low serotonin. Therefore testosterone concentrations and aromatase activity appear to be positively correlated with overall aggressiveness, but not with measures of impulsivity. it is the low levels of serotonin in combination with high levels of testosterone or aromatase which increase intensity of aggressive response. So depending on the individual dog, one dog might be more competitive than another dog, one dog might be more impulsive than another dog (Birger et al 2003).

Fights over access to territories resources and social status occur frequently in the males of most mammalian species. Independent males that compete differences in age, size, weight , and stamina play an important part of the outcome (Clutton-Brook et al 2013).

In most groups of dogs frequency and intensity of aggression in females is lower than in males, They use the same combination of visual, olfactory and vocal displays, and quality of signals, display their age, size and condition. Females will defend their territory from intruders and can be as aggressive as males and can lead to serious injury and death however female aggressive displays are usually directed at rivals. (Sherman et al 1996; Wrubel et al 2011). This type of aggression can begin around the time of sexual maturity to adulthood.

Fear aggression is a normal behaviour it is part of nature and affects a wide spectrum of causes of aggression: Stimuli that cause fear may be related to predators, intensive physical environmental stimuli and warning signals. Fear can sometimes be observed due to constitutional factors or temperament or in other cases because of insufficient experience with fearful stimuli (Overall 2013; Beaver 2010; Landsberg et al 2013). According to Hediger (1965) critical distance encompasses a narrow zone separating flight distance from attack distance, a dog might flee an approaching person/animal until it meets a barrier, if the person/animal continues to approach and the dog is cornered the dog is likely to attack. Effective socialisation will decrease critical distances, however some dogs despite good practices will be predisposed to maintain a distance (Hall 1969,1990; Coppinger et al 1996).

Dominance aggression, has definitions varying with nearly every A dog displaying aggression can display it self-confidently (dominant behaviour) however a dog that needs to control regardless of context is neither adaptive or normal. It is important not to blur the lines between normal behaviour i.e. the dog perceives he or his resources are at risk which is adaptive, or abnormal behaviour where there is no risk to the aggressor (Overall 2005). In addition a dog that has to control everything is not an evolutionary stable strategy (Dawkins 2006) and as a result true dominance aggression is rare (Overall 2013). Overall (2013) describes dominance aggression as a conflict aggression and is characterised by consistent atypical, out-of-context aggressive behaviour directed towards people. These behaviours include growling, snapping, and biting. Bites are usually not preceded by a vocal warning.

Frustration- elicited aggression The frustration-aggression hypothesis was proposed by Dollard et al (1939). According to this view, frustration, which is defined as "the state that emerges when circumstances interfere with a goal response," this can apply to the frustration that a dog feels when he can see but not reach his goal. This frustration occurs because there is a window, door, fence or a lead which prevents him achieving his goal, this often leads to aggression, fence fighting, lunging etc. This type of aggression occurs in both puppies and adults (Overall 2013 Beaver 2009 Landsberg et al 2013).

Redirected aggression is a lot like frustration-elicited aggression withthe exception that the dog need not be frustrated. Redirected aggression occurs when a dog is aroused by or displays aggression toward a person or animal, and someone or something else interferes with it. The dog redirects the aggression from the source that triggered it to the person or animal who has interfered with it . This is why people are often bitten when they try to break up dog fights. Another example is when two dogs are barking at someone from behind a fence, and one will turn and attack the other. Male and female dogs are equally prone to redirected aggression, and this type of aggression occurs in both puppies and adults (Overall 2013 Beaver 2009 Landsberg et al 2013).

Impulsive reactive aggression, Impulsivity is a trait related to inhibitory control Impulsive individuals show a decreased ability to tolerate delay of reinforcement (Lyndsay 2000). Impulsive aggression, is a lot like frustration-elicited aggression with the exception that the dog is being reactive; lacks self control and with the inability to control associated emotions (Abrantes 2005). Impulsive behaviour has been linked to decreased levels of serotonin and dopamine in a number of species. In domestic dogs, impulsivity is implicated in problem behaviours that result from a lack of self control this type of aggression occurs in both puppies and adults (van Rooney et al 2014).

Pain-Elicited Aggression An otherwise gentle, friendly dog can behave aggressively when in pain. A dog with a painful condition or an infection might bite with little warning, even if the reason they are being touched is to help the dog. Use of certain pieces of training equipment, such as the choke/prong / shock collars can inflict pain on a dog and prompt a pain-elicited bite to the handler. Male and female dogs are equally prone to pain-elicited aggression, and this type of aggression can occur in both puppies and adults (Overall 2013 Beaver 2009 Landsberg et al 2013).Relief of pain is important for reduction of misdirected aggression (Jenson 2007).

Loss of Rapid Eye Movement (REM) atonia leads to REM Sleep Behavioural Disorder (RBD) which causes dream enactment. If the dog is having combative dreams it can lead to vigorous and violent behaviours resulting in attacking the nearest object, person or animal. Most patients do not have structural lesions of the pons, but the disorder is thought to arise from an imbalance of neuronal regulation in this area,which is responsible for regulating REM and nREM sleep. The semi- purposeful behaviour with confusion may be impossible to distinguish from seizures or postictal behaviour. Unlike most partial seizures, REM behaviour disorder will be restricted to sleep. (Kaplin et al 2005: Brown et al 2012).

Medical problems should be considered for aggression : implicated in aggression are Hypothyroidism, epilepsy, metabolic disorders, Rabies ; Distemper, neoplasia, Hydrocephaly, hepatic disorders, endocrine disorders, poisoning amongst others (Kotteforovi et al 2008;Beaver 2009; Overall 2013; Landsberg et al 2013).

Drugs Certain medications could give rise to aggression. Selective serotonin re uptake inhibitor ( Prozac fluoxetine etc)   can result in paradoxical reactions resulting in increased aggression
towards individuals and so can Benzodiazepines, Barbituates, Chlorpromazine etc (Maddison et al 2008).

Nuture A deprived socio-cultural environment where both humans and their dogs are exposed to the same suboptimal conditions eg; homelessness (Gross et al 2004)

Punishment based training is more likely to result in a dog aggressing towards humans (Casey et al 2014)

Inconsistency in ownership style could also result in a dog aggressing towards humans. For example being allowed on the sofa one minute, being shouted at to get down next. Having food or valuable resources taken away constantly could result in a dog aggressing towards humans.

Constantly being disturbed whilst trying to sleep on his bed could result in the dog aggressing towards the person who disturbed him.

 In appropriate socialisation and insufficient exposure to humans and or other species. If the dam is aggressive towards humans the chances are the puppy will also be aggressive towards humans (Overall 2013; Beaver
2009).

Learning is also an important factor in the development of aggressive behaviour. The dog learns to be aggressive in order to achieve a goal, following the principal of instrumental conditioning, daily encounter s of the dog with people, can produce an important impact in the development of aggressiveness (lansdsberg et al 2013; Overall 2013).

Heritability of aggressive traits: Humans have selected behaviours in dogs for hundreds of years, and exploited the predatory sequence, Schavbert (2006) suggest that breeding selection for dog show use is positively correlated with social and non-social fearfulness, and negatively with playfulness, curiosity in potentially threatening situations and aggressiveness, whereas selection for working dog use is positively correlated with playfulness and aggressiveness. Furthermore, correlation analyses show that popular breeds have higher sociability and playfulness. However if you look at how the pedigree breed standard was developed for the Staffordshire Bullterrier. The full wild canine predatory sequence is: orient>eye>stalk>chase>grab bite>kill bite>dissect>consume (Udell 2014). Breeders of the Staffordshire bull terrier selected for the hypertrophied grab bite, which gave them their distinctive jaw and facial structure.

“The extraordinary features of a bully breed are reminiscent of the bull-baiting tactics and strategies, it made the Bulldog deadly effective in killing a bull. The quagmire of dogs, fighting bulls was intense and the way dogs used to grab the bulls nose needed some special features that could help in sticking to the bull’s nose to kill him. The Bulldogs were trained to crouch low to the ground to shield their bodies from the bull’s horns when it charged. The shoulders were placed on the outside of the body, the hind quarters of the Bulldog are not as well developed as the fore quarters, allowing the dog to be shaken violently without suffering any spinal injuries, The head of the Bulldog, like his body is also the part of the fighting strategies that men wanted to develop. The short jaws, lower jawbone is longer than the upper jawbone which allows the dog to hang onto whatever it wants with a surprising tenaciousness. The grip is very strong, and the structure of the jaws, surprisingly enables the dog to move jaws in a manner that it can hang onto the throat of the bull and shred the flesh, sinew, and muscle until it reaches the jugular. The Bulldog continues to hang on until the bull is brought down; bleeding to death. The skin folds on the face allow the Bull’s blood to flow down the dogs face under its chin rather than into its eyes. The Bulldog has a short snout on the upwards face to allow breathing, while retaining its grip on the bull’s nose. The bull is, in the meantime suffocating due to the loose jowls of the bulldog blocking the passage of air” (Page 15 Jenkins et al 1997).

The breed standard for the Staffordshire Bullterrier was developed to prevent the breed from ‘softening’ (Morris 2008; Jenkings et al 1997; Catherine 2011), If humans select for temperament the destabilizing effect of selection will result in changes to the phenotype and therefore not match the profile of the breed standard (Baelev 1979). Baelev suggest that the interface of physical and behavioural conformation means it is not possible to breed out aggressive behaviour of fighting dogs while retaining their shape and appearance. However it is clear that not all Staffordshire bullterriers carry the aggressive trait to make good fighting dogs (Jenkins 1997). Canine experts generally deny the existence that there is an automatic link between breed and aggression, but they point towards the existence of particular aggressive breeding lines (Serpell et al 2014), but even perfect breeding lines produce 'misfit' puppies (Coppinger et al 1988).

When it comes to assessing aggression It is not necessary to  see a dog doing the aggressing, and consequently giving the dog more practice at the behaviour. So roles should be more  of a  preventative model and the use of a good assessment tool that can identify triggers possibly use of video recordings. For example if the person referred says their dogs bark lunge or attack people coming into the house, but are fine out of the house, behavioural modification programme would begin away  from the environment that could trigger an aggressive response begin getting the skills in place before working in that environment.

It is clear from the above terms aggression, they can be applied to a variety of causes. Human directed aggression is not correlated with dog directed aggression but the cause of either human directed aggression or dog directed aggression or any other type of aggression can be due to nature , physiological disorders , neurological disorders, medical disorders, drugs , nurture, environment and any of the multitude of categories stated above. Therefore treatment of aggression includes identify the trigger, Eliminate all triggers, if you cant eliminate triggers manage it through well placed barriers, careful use of space and distance, good practice of resources, prevent from practicing the behaviour; and use desensitisation and counter-conditioning, satisfy the needs of the dog, and confidence building exercises. Occasionally re-homing is the best option particularly if it is a sex related aggression or owners are not able to manage and continue behavioural modification. And occasionally euthanasia might be the best option for the welfare of the dog and for safety of others.

We can use a functional definition of aggression but this adds our interpretation of the function of the animal’s so-called intent and as a result it focuses on the individual, but it forgets about the survival and fitness of the species and others. In addition is the interpretation actually related to the aim and function of the dogs behaviour, for example does chase behaviour have anything to do with predatory aggression or territorial, If it is unrelated to the aim and function, then our functional classification makes no sense. Many forms of behaviour contain representations of a desired end-point (Nelson 2006). If this is true, then we have to seriously consider cognition in the dog.

References and further reading

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Birger, M. Swartz,M. Cohen, D. Alesh,Y. Et al (2003) Aggression: The Testosterone-Serotonin Link Review article. Israel Medical Association Journal Vol 5 . Sept 2003 pp  653-658

Bradshaw, J.W.S. & Nott, H.M.R. 1995 Social and Communication Behaviour of Companion Dogs. In; Serpell, J.A. (Ed) The Domestic Dog; Its Evolution, Behaviour and Interactions With People. Cambridge University Press.

Brown, R.   Basheer, R.  McKenna. J. ,  Strecker, R , . McCarley, R, (2012) Control of Sleep and Wakefulness Physiological Reviews Published 1 July 2012 Vol. 92no. 1087 1187DOI: 10.1152/physrev.00032.2011. Avaliable from: http://physrev.physiology.org/content/92/3/1087

Casey, R. Loftus, B.  Bolster, C. Richards, G. Blackwell, E. (2014)  Human directed aggression in domestic dogs (Canis familiaris): Occurrence in different contexts and risk factors Applied Animal Behaviour Science vol:152 pp 52-63.

Catherine, M. (2011) “Bulldog breeds” Website of Bull dog information library. Catherine Marion-deluca 2003-2011 accessed (06/03/2015. http://bulldogbreeds.bulldoginformation.com/different-bulldog-breeds-types.html

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