Using the mini C-BARQ to investigate the effects of puppy farming on dog behaviour
Introduction
Dogs are the most common type of pet (PFMA, 2017) and dog ownership increases with number of household members and if children are present (Downes et al., 2009), suggesting that dogs often play an important role in a family context. Dogs have been found to have a beneficial impact on children's emotional development (Vidović et al., 1999), provide emotional support (Hawkins et al., 2017), and increase physical health in old age (Curl et al., 2016). However, problematic or extreme canine behaviours may hinder the positive role a dog can have: perceived problems like aggression and house soiling can precipitate increased family tensions (Power, 2008), while destructive tendencies and aggression are the most common reason for dogs to be relinquished to shelters (Diesel et al., 2010). Understanding how to reduce problematic behaviours is therefore important both in a family context and for dog welfare, but research on dog breeding, the environment it creates for early development, and the long-term behavioural implications is only starting to receive attention.
Intensive dog breeding (IDB) can take a range of forms and has been given various names, such as 'puppy mills', 'puppy farms', or Commercial Breeding Establishments (CBEs). IDB tends to occur where an increased demand for dogs makes breeding a lucrative business, often to the detriment of dog welfare, where animals are kept in cramped, overpopulated conditions, and are selected as breeding stock irrespective of behaviour or health. Studies in the United States have shown CBEs have quite serious negative effects on adult dog behaviour, noticeably for fear and aggression (McMillan et al., 2013). However, IDB operations are poorly defined on an international scale as terminology is inconsistent: these sometimes refer simply to larger breeding operations, and sometimes to breeding operations specifically harmful to welfare. As a result, it can be difficult to build a global understanding of the effects of these practices, which will vary in their legality, the regulations applied, and consequently the welfare of animals. In line with current UK terminology (Scottish SPCA, 2018), and in order to underline the detrimental welfare effects and often illegal nature of these practices (rather than their scale), we will refer to IDB operations detrimental to welfare as puppy farming (see Everett, 2014 for a discussion of ethical terminology regarding puppy farming).
Over the last 30 years, puppy farming has created both legal and public concern in the UK, especially as accumulating evidence suggests puppy farming has significant costs, both in terms of animal welfare and for the families whose pets display health and behavioural issues. This problem has started being addressed with legislation regulating welfare and breeding practices,1 and with the trial of an assured breeder scheme in Scotland (Scottish SPCA, 2018). Although stricter regulation has probably reduced the number of legal IDB operations detrimental to dog welfare, it means that intensive breeders may choose to operate outside legislation (possibly operating with even worse welfare conditions) or that dogs will be imported from other countries with less stringent regulation (Dog Trust, 2017). However, the mechanisms through which these intensive breeding practices influence dog behaviour are only starting to be investigated (McMillan, 2017), and there is little evidence concerning which aspects of puppy farming are most deleterious to canine behaviour and health, or how to mitigate the negative outcomes associated with puppy farming.
In a review of evidence, McMillan (2017) argues that behavioural differences between intensively bred dogs and those from other sources can be traced back to a combination of genetic, prenatal, and developmental factors. These are poorly managed in puppy farms, raising a series of concerns for the behaviour of those dogs as adults, and for their welfare (HSVMA, 2013).
Bitches are often bred continuously until they are no longer able to deliver puppies and are then discarded. Intensive breeding affects the bitch's health, immune function and ability to care for her pups. McMillan et al. (2011) demonstrated that breeding dogs in CBEs developed fears and phobias and learning deficits. These issues may transfer directly to the puppies, as studies have demonstrated that higher quality maternal care in dogs will tend to increase puppy social and physical engagement (Foyer et al., 2015), may aid positive interest in humans (Guardini et al., 2017), and that puppies may also learn to display certain behaviours from their mothers (Lord, 2010).
On the genetic side, careful breeding remains an effective way of influencing dog behaviour and health. A wide variety of dog behaviours have been studied for their heritability, such as aggression (Pérez-Guisado et al., 2006), anxiety (Goddhard and Beilharz, 1983), or human-directed social behaviour (Persson et al., 2015), a process which has been made more precise since the mapping of the dog genome in 2005. Mandatory behavioural screening of pedigree parents has managed to successfully reduce aggressive temperaments in breeds such as Dobberman and Rottweiler (van der Borg et al., 2017). Likewise, screening the parents and avoiding reproduction of ailing individuals can significantly weed out congenital illnesses or deformities. Such behavioural and physiological screenings are not likely to be performed in puppy farms, suggesting that genetically-caused behavioural and medical issues are not likely to be addressed.
Developmentally, puppy farming affects the welfare of puppies because it does not provide an appropriate environment for canine behavioural development. Dogs have a set of six relatively well-defined stages of behavioural development (Serpell et al., 2016). During these sensitive periods, the puppy farming environment may adversely affect puppies' behavioural development, especially during first four stages: prenatal, neonatal, transitioning, and socialisation.
During the prenatal period, developing pups are influenced by maternal levels of cortisol and androgen, which has been linked to increased stress sensitivity among rats and foxes (Champagne, 2008; Braastad, 1998). Maternal stress in rodents also affects the amount of care pups receive in the neonatal period (first two weeks), which has long-term consequences for their regulation of their Hypothalamic-Pituitary-Adrenal (HPA) axis (Champagne et al., 2003). The high levels of stress bitches are likely subjected to in puppy farms will therefore have direct and systematic deleterious effects on the puppies, both prenatally and during the neonatal period.
The transition period, in the third week, marks the maturation of puppies' sensory systems (opening of their eyes and then their ear canals) until the onset of motor development in the fourth week, signalling the onset of the socialisation period. It is during this exploratory socialisation period (4 to 12 weeks), that puppies are most directly influenced by their environment. During this period, it is crucial that pups are exposed both to the human and environmental factors that they are likely to interact with, as they may otherwise never fully habituate (Scott and Fuller, 1965). Variations in socialisation timing can partially explain behavioural differences amongst breeds, subtle differences that puppy farmers are unlikely to take into account. For example, German Shepherd puppies show stronger novelty avoidance at 5 weeks than Labradors, who are more flexible and retain the opportunity to socialise in their new home for longer (Lord et al., 2016). Puppy farming affects the patterns of socialisation in three ways: firstly, the kennel environment contains a narrower range of stimuli and reduces human contact. Since dogs also form 'localisation' attachment (Scott and Fuller, 1965), this suggests that dogs from kennels will show increased fear responses as adults both to humans and their environment (Appleby et al., 2002). Secondly, dogs are unlikely to be socialised properly, or according to the needs of their breed. Finally, puppies are often sold at or before eight weeks of age, during one of the most sensitive developmental phases; if puppies are shipped from overseas, long transportation will translate to high stress levels and have long term effects on behaviour.
Welfare issues continue after intensively bred dogs are bought as pets, because both health and behavioural issues increase the likelihood that a dog will be relinquished to a shelter (Duffy et al., 2014). Based on anecdotal evidence, the UK Kennel Club states that "puppies bred by puppy farmers are more likely to suffer from common, preventable, infectious diseases, painful or chronic inherited conditions, behavioural issues and shorter life spans". Our research will scientifically investigate these claims.
The first aim of this research was to investigate different ways of measuring the effects of puppy farming. This was done by validating four short new scales developed with the Scottish SPCA, and validating the use of the mini C-BARQ (Duffy et al., 2014) with the current sample. In order to maintain statistical power in further analysis, Exploratory Factor Analysis (EFA) was used to determine whether the mini C-BARQ could be validly condensed along latent behavioural dimensions.
The second aim was to investigate the effects of puppy farming on medical health and behaviour. The investigation of behaviour attempted to replicate the results of McMillan et al. (2013), who used the C-BARQ (Hsu and Serpell, 2003) to demonstrate the negative effects of intensive breeding on various behaviours including aggression, fear, separation anxiety, and a variety of other behavioural problems. The current research aimed to reproduce their results within the UK context, although we note a few differences. First, rather than using the full-length C-BARQ, the current study used the mini C-BARQ (Duffy et al., 2014), which allowed for additional questions to be included without making survey length prohibitive, probing aspects such as the living conditions of the dog at purchase, and their health condition. Second, the questionnaire was advertised through a different set of routes and may have reached a different participant sample: while McMillan et al. advertised through veterinary practices, the current research advertised primarily through animal rehoming centres, welfare charities, and social media. Finally, this study used a different set of comparison groups: while McMillan compared breeder-obtained dogs (excluding home-bred, rescued, or dogs obtained from a friend/relative) to pet-store bought dogs (proxy for CBEs), the current study compared dogs categorised as coming from puppy farms to those from any other sources. Despite these differences, we hypothesised similar effects would be found in the current study: dogs from puppy farms will be found to score significantly worse on most, if not all, of the mini C-BARQ measures.
The third aim was to explore how basic measures taken by the owner could mitigate the effects of poor early life experience. Research has demonstrated that different types of training, such as puppy classes, can significantly improve the behaviour of dogs (Kutsumi et al., 2013). Little research has been carried out for other simple measures, such as whether the frequency of dog walking can improve behaviour. We hypothesised that both dog walking and dog training will decrease the incidence of negative behaviours as measured by the mini C-BARQ.
Section snippets
Design
This research used a cross-sectional online questionnaire-based survey design. A self-report questionnaire was designed consisting of standardized and newly developed measures and distributed using Bristol Online Survey. The online questionnaire was open from the 7th of June to the 27th of July 2017.
Participants
Participants were recruited through a combination of non-probability sampling methods (i.e. where the sample may not be representative of the general population because of biases potentially
Scale reliability and analysis
All scales except the 'Owner Care' had α above 0.7, and so were retained (see Table 1). Sub-items in the 'Owner care' scale were investigated separately. It was found that the question "Does your dog obey basic commands (sit, stay, down, etc.)?" was highly skewed, with 96% of respondents reporting 'yes'. As a result, this item was removed, and two possible subscales each with two items remained. Because these two subscales only had two items each, the Spearman-Brown split-half reliability
Scales measuring the effects of puppy farming
The first aim of this research was to investigate the validity of both established and new scales for measuring the effects of puppy farming on dog behaviour and health.
Conclusions
Puppy farming has a negative effect on 11 of 14 subscales of the mini C-BARQ, and on both medical health scales measuring infectious and chronic illnesses. A variety of new measures have been developed that might help measure the effects of poor early life experience in dogs. Although walking and training were both found to have an effect on reducing mini C-BARQ score, more research is necessary to determine the nature of this relation. Overall, these results confirm the impact of puppy farming
Acknowledgements
The authors would like to thank all the organisations which forwarded and publicised the questionnaire and allowed a wider pool of participants to be reached. This research did not receive any specific grants from funding agencies in the public, commercial, or not-for-profit sectors.
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