CS-14-133-Best-Friends-Animal-Society - Oshawaapp.oshawa.ca/agendas/.../06-19/CS-14-133-Best-Friends-Animal-Soc… · Angeles, Chicago and San Diego), ... and puppies from commercial

12 June 2014

Oshawa City Council 50 Centre Street South Oshawa Ontario L1H 3Z7

Re Consideration of a Pet Sales Bylaw

Dear Mayor Henry and members of the Council

On behalf of Best Friends Animal Society a national animal welfare organization in its thirtieth year I would like to offer our support for a bylaw to restrict the retail sale of dogs and cats in Oshawa pet stores We urge you to join the 57 communities throughout North America that have made the change to no longer allow pet stores to sell commercially bred companion animals unless the animals come from shelters or rescue groups

Pet mills particularly puppy mills are a serious problem These facilities which supply nearly 100 of retail pet stores and online retailers are cruel and inhumane facilities in which profit and maximum productivity take priority over the welfare of the animals

These types of kennels often have hundreds of dogs in one facility confined to very small cages for their entire lives breeding continuously in order to produce as many puppies as possible for the pet trade

Because the goal is to make a profit pet mill owners must cut corners to keep expenses low and profits high For the unsuspecting consumer this frequently results in the purchase of a pet facing an array of immediate veterinary problems or harboring genetic diseases that surface down the line This creates a financial burden on the consumer and results in many of these animals being surrendered to overcrowded shelters

It makes little sense to continue manufacturing dogs and cats when so many are being killed for lack of space Public education has been effective but until communities take the initiative to limit the supply of pets being imported from substandard commercial facilities there can be no hope of preventing these unnecessary deaths

Those who benefit most from companion animal sales in pet stores are the retailers themselves While they may profit from the practice of buying these pets at a low price from commercial brokers and then selling them (typically without first spaying or neutering them) at a high price it is the taxpaying public who pays for animal control to house and kill unwanted animals in the community

CS-14-133

69

Pet stores that sell commercially bred animals can be part of the solution rather than the problem simply by either stopping pet sales altogether (and focusing on other profitable ancillary components such as grooming daycare or pet supplies) or by changing to a business model that offers products services and space for animal rescue organizations to adopt out animals from their stores

Best Friends has partnered with several of the many pet stores that have transitioned from selling milled dogs and cats to offering rescued pets for adoption and we have found this ldquohumanerdquo model to be both viable and embraced by the communities in which the stores are located Thus a restriction on the retail sale of pets would not preclude pet stores from staying in business and could in fact alleviate a significant burden on the city by increasing pet adoptions

The intent of the pet sales ordinances that have been enacted thus far is to focus on the most inhumane and irresponsible of the breeders who supply the pet trade the high volume commercial mills Not only are responsible hobby breeders not negatively impacted by these ordinances the ordinances actually help them by eliminating the wholesale market for poorly bred animals giving them increased opportunity to provide a better quality of ldquoproductrdquo for people looking to purchase pets

Best Friends and our members thank you for taking a compassionate common sense initiative to addressing the pet mill crisis in your community and setting a positive example for the rest of the country to follow We have been proud to work with many of the municipalities throughout North America that have enacted similar ordinances (including Los Angeles Chicago and San Diego) and we are proud to support you in your efforts as well I hope you will let us know if there is anything we can do to help further this critical reform

Thank you for your consideration of this important proposal

Respectfully

Elizabeth Oreck Elizabeth Oreck National Manager Puppy Mill Initiatives Best Friends Animal Society puppymillsbestfriendsorg elizabethobestfriendsorg

70

Executive Summary Scientific studies of dogs and puppies from commercial dog-breeding establishments (puppy mills)

BACKGROUND Commercial breeding establishments or puppy mills are large-scale facilities where dogs are confined in small enclosures for their entire reproductive lives with little to no exercise or positive human contact The sole purpose of such facilities is to mass-produce puppies to sell them for profit through retail pet stores and via the Internet

SYNOPSIS In two large-scale studies of dogs from high-volume commercial breeding establishments (one study focusing on the adult breeding dogs and the other on the puppies sold through pet stores) the evidence showed conclusively that these breeding facilities are highly injurious to both groups of dogs resulting in severe extensive and longshyterm harm to the behavioral and psychological well-being of the dogs

Study 1 The adult breeding dogs WHAT THE STUDY LOOKED AT This study compared a wide array of psychological and behavioral characteristics of 1169 dogs formerly kept for breeding purposes in commercial breeding establishments with pet dogs owned by members of the general public

RESEARCHERS Franklin D McMillan DVM Best Friends Animal Society Deborah L Duffy PhD University of Pennsylvania School of Veterinary Medicine James A Serpell PhD University of Pennsylvania School of Veterinary Medicine

THE PUBLISHED PAPER Mental health of dogs formerly used as lsquobreeding stockrsquo in commercial breeding establishments FD McMillan DL Duffy JA Serpell Applied Animal Behaviour Science 2011 135 86-94

WHAT THE STUDY FOUND

bull The results showed a broad range of abnormal behavioral and psychological characteristics in the former breeding dogs from large-scale commercial breeding establishments including significantly elevated levels of fears and phobias pronounced compulsive and repetitive behaviors such as spinning in tight circles and pacing house soiling and a heightened sensitivity to being touched and picked up

bull The psychological harm demonstrated in these dogs is severe and long-lasting Much of the harm is irreparable and will remain a continued source of suffering for years after the dogs leave the breeding facility in some cases for the entire lifetime of the dog

71

CONCLUSIONS

bull Current laws at both the national and state levels are not based on current scientific knowledge of animal psychology quality of life suffering and welfare and are thus inadequate to protect dogs from the psychological harm resulting from living in commercial breeding establishments

bull Legislation to adequately protect the welfare of dogs in confinement needs to be updated to reflect current scientific knowledge

To obtain a copy of the published study contact Dr Frank McMillan (drfrankbestfriendsorg)

Study 2 The puppies WHAT THE STUDY LOOKED AT This study compared the psychological and behavioral characteristics of 431 adult dogs who were purchased as puppies from pet stores with adult dogs purchased as puppies from small-scale private breeders

RESEARCHERS Franklin D McMillan DVM Best Friends Animal Society James A Serpell PhD University of Pennsylvania School of Veterinary Medicine Deborah L Duffy PhD University of Pennsylvania School of Veterinary Medicine Elmabrok Masaoud PhD Atlantic Veterinary College University of Prince Edward Island Ian Dohoo DVM PhD Atlantic Veterinary College University of Prince Edward Island

THE PUBLISHED PAPER Differences in behavioral characteristics between dogs obtained as puppies from pet stores and those obtained from noncommercial breeders FD McMillan JA Serpell DL Duffy E Masaoud IR Dohoo Journal of the American Veterinary Medical Association 2013 242 1359-1363

WHAT THE STUDY FOUND

bull Dogs obtained as puppies from pet stores received significantly less favorable scores than breeder-obtained dogs on most behavioral variables measured Compared with dogs obtained as puppies from noncommercial breeders dogs from pet stores had significantly greater aggression toward human family members unfamiliar people and other dogs greater fear of other dogs and typical life events and greater separation-related problems and house soiling

bull For no behavior evaluated in the study did pet store dogs score more favorably than noncommercial breeder dogs

bull The chances of a dog developing serious behavior problems is much higher for dogs purchased as puppies from pet stores as compared to dogs obtained from small noncommercial breeders

CONCLUSIONS

bull On the basis of these findings combined with findings from earlier small-scale studies of dogs obtained from pet stores until the causes of the unfavorable differences detected in this group of dogs can be specifically identified and remedied the authors of this study withhold any recommendation that puppies be obtained from pet stores

2 72

bull Dogs sold by pet stores are misrepresented to consumers as a high-quality product because the data now shows that consumers are not receiving what they believe they are paying for The increased risk of behavior problems that pet store customers face as their dog matures includes aggression issues which pose a significant risk of human injury Consumer protective legislation is urgently needed in this area

bull Legislation to improve the conditions in the large-scale commercial breeding facilities supplying puppies to pet stores is needed to assure that the puppies are not at any increased risk of maturing into adult dogs with serious behavior problems

To obtain a copy of the published study contact Dr Frank McMillan (drfrankbestfriendsorg)

Overall Conclusions

bull Current laws provide inadequate protection against harm to breeding dogs and puppies associated with commercial breeding establishments

bull Consumers purchasing puppies from pet stores are unknowingly assuming a risk of difficult and serious behavior problems in their dogs including dog behavior that can endanger their own safety

bull If dogs are to be bred to produce puppies for sale all of the dogs and puppies should be assured a decent quality of life based on the most current scientific research

For More Information For more about Best Friends Animal Society go to bestfriendsorg To learn about Best Friendsrsquo puppy mill initiatives and what you can do to help visit puppymillsbestfriendsorg

3 73

Differences in behavioral characteristics between dogs obtained as puppies from pet stores and those obtained

from noncommercial breeders

Franklin D McMillan DVM DACVIM James A Serpell PhD Deborah L Duffy PhD Elmabrok Masaoud PhD Ian R Dohoo DVM PhD

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ObjectivemdashTo compare the owner-reported prevalence of behavioral characteristics in dogs obtained as puppies from pet stores with that of dogs obtained as puppies from noncommercial breeders DesignmdashCross-sectional study AnimalsmdashDogs obtained as puppies from pet stores (n = 413) and breeder-obtained dogs (5657) ProceduresmdashBehavioral evaluations were obtained from a large convenience sample of current dog owners with the online version of the Canine Behavioral Assessment and Reshysearch Questionnaire which uses ordinal scales to rate either the intensity or frequency of the dogsrsquo behavior Hierarchic linear and logistic regression models were used to analyze the effects of source of acquisition on behavioral outcomes when various confounding and intervening variables were controlled for ResultsmdashPet storendashderived dogs received significantly less favorable scores than did breeder-obtained dogs on 12 of 14 of the behavioral variables measured pet store dogs did not score more favorably than breeder dogs in any behavioral category Compared with dogs obtained as puppies from noncommercial breeders dogs obtained as puppies from pet stores had significantly greater aggression toward human family members unfamilshyiar people and other dogs greater fear of other dogs and nonsocial stimuli and greater separation-related problems and house soiling Conclusions and Clinical RelevancemdashObtaining dogs from pet stores versus noncommershycial breeders represented a significant risk factor for the development of a wide range of unshydesirable behavioral characteristics Until the causes of the unfavorable differences detected in this group of dogs can be specifically identified and remedied the authors cannot recomshymend that puppies be obtained from pet stores (J Am Vet Med Assoc 20132421359ndash1363)

It has long been an article of faith among veterinarians ABBREVIATIONS and canine professionals that dogs obtained as puppies C-BARQ Canine Behavioral Assessment from pet stores have a higher prevalence of health and be

and Research Questionnaire havioral problems1 However there has been a dearth of CBE Commercial breeding establishment empirical studies to support this notion In a retrospective NCB Noncommercial breeder survey of the owners of 737 adult dogs Jagoea found that

dogs obtained from pet shops had a significantly higher prevalence of owner-directed (dominance-type) aggres by owners in a convenience sample of 413 companion sion and social fears (fear of strangers children and unfa dogs of which 47 were obtained from pet stores Remiliar dogs) than did dogs from 5 other sources breeders sults indicated that dogs purchased from pet shops or animal shelters friends or relatives found or rescued off shelters were considered by their owners to be more the streets and home bred (ie bred and reared in the cur unfriendly or aggressive than were dogs purchased from rent ownerrsquos home)2 However the sample size of pet store breeders and significantly more nervous than dogs bred dogs in that studya was small (n = 20) by the present owner However by using broadly de

Bennett and Rohlf3 investigated the frequency of fined behavioral subscales rather than discrete behavpotential problematic behavior patterns as reported iors the researchers were not able to ascertain whether

pet shop dogs had specific problematic behaviors more From the Best Friends Animal Society 5001 Angel Canyon Rd Kanab frequently than did dogs from other sources

UT 84741 (McMillan) the Department of Clinical Studies-Phila Mugford4 reported analyzing a sample of 1864 delphia School of Veterinary Medicine University of Pennsylva dogs with various behavioral problems and determined nia Philadelphia PA 19104 (Serpell Duffy) and the Department that ldquoonly 10 of purebred dogs obtained directly from of Health Management Atlantic Veterinary College University breeders presented separation-related problems whereof Prince Edward Island Charlottetown PE C1A 4P3 Canada (Masaoud Dohoo) as 55 of purebred dogs originating from so-called

Supported by a grant from the Animal Welfare Trust lsquopuppy farmsrsquo or lsquopuppy millsrsquo present such problemsrdquo Address correspondence to Dr McMillan (drfrankbestfriendsorg) Sample sizes and the way in which it was determined

JAVMA Vol 242 No 10 May 15 2013 Scientific Reports 1359

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that the dogs came from puppy farms or puppy mills were not reported

Some inconsistent findings have also been reported Pierantoni et al5 compared owner-reported behaviors between 70 adult dogs separated from their litters at 30 to 40 days of age and 70 adult dogs separated from their litters at 2 months of age Their analysis included the source of the dog classified into 3 categories breeder pet shop or friend or relative The researchers found no significant association between the source of the dog and the behavioral categories examined In a study of the efficacy of a dog-appeasing pheromone in reducing stress associated with social isolation in puppies recently acquired from pet stores Gaultier et al6 noted that their data did not seem to support the hypothesis that puppies from pet stores constitute a special at-risk population for the development of behavioral problems The researchers reported that the puppies in that study6 (n = 66) did not appear to disturb their owners any more than those in a previous study by Taylor and Mills7 involving puppies acquired from local pedigree dog breeders However the breeders in the latter study7 included a semicommercial breeder and at least 1 puppy millb

Most puppies sold by pet stores in the United States are purchased from brokers who may themselves be breeders but overwhelmingly acquire their puppies from high-volume breeding facilities or CBEs located throughout the United States8 Conditions in the CBEs which supply tens of thousands of puppies to retail pet stores each year vary widely Conditions in CBEs range from modern clean and well-kept to squalid noxious and gravely detrimental to animal health and welfare9ndash11

The purpose of the study reported here was to evaluate the hypothesis that dogs obtained as puppies from pet stores would be reported to have an increased prevalence of behavioral problems compared with dogs obtained as puppies from NCBs

Materials and Methods

Data collectionmdashBehavioral evaluations of the dogs were obtained by use of the online version of the C-BARQ a standardized survey instrument with established reliability and validity characteristics12 The C-BARQ is designed to provide quantitative assessments of a wide array of behavioral characteristics of dogs and has been widely used as a research tool for comparing behavior in different dog populations13ndash15 The questionnaire consists of 100 items that ask respondents to indicate on a series of 5-point ordinal rating scales their dogsrsquo typical responses to a variety of everyday situations during the recent past The scales rate either the intensity (aggression fear and excitability subscales) or frequency (all remaining subscales and miscellaneous items) of the behaviors with a score of 0 indicating the absence of the behavior and a score of 4 indicating the most intense or frequent form of the behavior The C-BARQ currently comprises 14 behavioral factors or subscales and a further 22 miscellaneous stand-alone items Higher scores are generally less favorable for all items and subscales with the exception of trainability for which higher scores are more desirable Owners were also asked to indicate

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the dogrsquos current age at the time the survey was completed whether there were other dogs living in the same household and whether the dog was used for specific working or recreational roles including breeding or showing field trials or hunting other sports (eg agility racing or sledding) and working roles (eg search and rescue service or sheep herding) To obtain information on the source from which the dog was acquired owners were also asked to respond to the question ldquowhere did you acquire this dogrdquo Possible responses included the following bred himher myself from a breeder from a shelter or rescue group from a neighbor friend or relative bought from a pet store adopted as a stray and other Consistent with the 2 previous studies3a that offered pet-owning participants the choice of breeder as the source of the dog the question in the C-BARQ regarding the source of the dog does not define the term breeder

SamplemdashThe online C-BARQ was advertised originally via an article in the newsmagazine of the Veterinary Hospital of the University of Pennsylvania and by notices sent to Philadelphia-area veterinary clinics and the top 20 US breed clubs as determined on the basis of American Kennel Club registrations Availability of the survey then spread via word of mouth No geographic limitations were applied and participation included residents of the United States as well as other countries A subset of these data consisting entirely of pet dogs whose owners reported obtaining them either from breeders (n = 5657) or pet stores (413) was used for analysis Breeder-obtained dogs were selected as the comparison group for the following reasons age at the time of acquisition would most closely match pet storendash obtained dogs for the most part breeder-obtained dogs are purebred as are those from pet stores and the life history of the dog prior to purchase in breeder-obtained puppies is relatively standardized thereby reducing the amount of environmental variability among the dogs of this group These assumptions apply to the United States and may have less validity in other countries

Statistical analysismdashTwo-level hierarchic linear or logistic regression models were used to analyze the data on behavioral measures16 The outcome variables (attachment and attention seeking chasing trainability excitability and energy) in the hierarchic linear model were treated as normally distributed continuous variables All other behavioral variables were dichotomized (eg 0 or gt 0) because they were typically highly skewed and it was impossible to identify a suitable transformation method to normalize their distribution These were analyzed with 2-level mixed logistic models Both types of model aimed to assess the relationship between source of acquisition (eg pet store vs breeder) and behavior while controlling for various confounding variables (other dogs in household working or recreational roles sex and body weight) or intervening variables (neutered vs sexually intact and age at the time of evaluation) All possible 2-way interactions between source of acquisition and confounding and intervening variables were explored and accounted for in the modeling process Nonsignificant confounding and intervening variables and interaction effects were removed from the

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1360 Scientific Reports JAVMA Vol 242 No 10 May 15 2013

75

model Breed was also included in both models as a ranshydom effect to account for clustering of dogs at the breed level Linear and logistic models were fit via restricted and full maximum likelihood estimation procedures The analysis was performed with statistical software17

by use of subject-specific modelscd For all comparishysons a value of P lt 005 was considered significant

Results

According to the results of the multiple regression analyses dogs acquired from pet stores differed signifishycantly from those acquired from breeders on 12 of 14 of the C-BARQ behavioral subscales In no category did pet store dogs have a more desirable score than breeder dogs (Tables 1 and 2) The strongest effects were observed in relation to aggressive behavior For example sexushyally intact pet store dogs were 3 times as likely to have owner-directed aggression as were sexually intact dogs acquired from breeders and pet store dogs were nearshyly twice as likely to have aggression toward unfamiliar dogs (dog-directed aggression) Pet store dogs were also 30 to 60 more likely to have stranger-directed aggresshysion aggression to other household dogs fear of dogs

and nonsocial stimuli separation-related problems and touch sensitivity In addition they were somewhat more excitable energetic and attention seeking and generally less trainable although this was only true for dogs that did not participate in working or recreational activities The only C-BARQ subscales that were not significantly different between pet store and breeder-derived dogs were chasing and stranger-directed fear In addition pet storendashobtained dogs had a range of miscellaneous behavshyioral problems at significantly higher frequencies than did those acquired from breeders (eg escaping from the home sexual mounting of people and objects and most forms of house-soiling)

Discussion

Results of this study supported the view that dogs obtained as puppies from pet stores are more likely to develop behavioral problems as adults compared with dogs obtained from NCBs The retrospective nature of the data used in this analysis did not permit determinations of causality However there are several potential explanations for the differences between pet store and NCB dogs

Table 1mdashResults of linear regression models comparing behavioral variables in dogs obtained from pet stores versus dogs obtained from NCBs

Other variables Variable controlled Predictor Effect 95 CI P value

Excitability 12346 PS 0204 012 to 029 lt 0001 Energy 12346 PS 0109 0004 to 021 0043 Chasing PS 0002 ndash013 to 010 0769 Attachment and 123456 PS 0204 012 to 029 lt 0001

attention seeking Trainability 123456 PSndashNot working dog ndash0195 ndash026 to ndash013 lt 0001

PSndash Working dog 0098 ndash007 to 027 0262

PS = Acquired from pet storeOther variables controlled were as follows 1 = other dogs 2 = dogs with working or recreational roles

3 = sex 4 = weight 5 = neutered 6 = age at time of evaluation (nonsignificant intervening variables [those variables that intervene the relationship between variable and predictor] were removed from the analyses)

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Table 2mdashResults of logistic regression models comparing behavioral variables in dogs obtained from pet stores versus dogs obtained from NCBs

JAVMA Vol 242 No 10 May 15 2013 Scientific Reports 1361

Variable

Separation-related behavior Owner-directed aggression

Stranger-directed aggression Nonsocial fear Dog rivalryDog-directed fear Dog-directed aggression Touch sensitivity Escapes from home or yard Rolls in odorous material CoprophagiaChews objects Mounts objects or people Urinates against objects

or furnishings Submissive urination Urinates when left alone Defecates when left alone

See Table 1 for key

Other variables controlled

123456 123456 123456 123456 12345 12346 12345

123456 123456 123456

12345 123456

123456 123456 12345

Predictor

PS PSndashNot neutered PSndashNeutered PS PS PS PS PS PS PS PS

PS

PS PS PS

OR

158 313 154 159 144 135 133 196 158 414 086 108 107 139 177

153 196 168

95 CI

119ndash211 187ndash523 116ndash206 118ndash216 101ndash207 105ndash174 103ndash171 144ndash267 118ndash211 175ndash983 067ndash109 086ndash136 084ndash136

11ndash175 132ndash239

113ndash207 152ndash152 131ndash216

P value

0002 lt 0001

0003 0003 0047 0021 0030

lt 0001 0002 0001 0214 0502 0590 0006

lt 0001

0007 lt 0001 lt 0001

76

The formative stages of the puppyrsquos life in the CBE are periods where stress may exert an impact on brain development Although no studies on sources of stress in CBEs or their potential effects on the well-being of the dogs have been published sources of stress have been investigated in dogs living in confinement in kennels18ndash21 animal shelters2223 and laboratories2425 Similar stressors have been documented in the CBE environment10 and it is therefore reasonable to suggest that the effects applied also to the dogs in the present study despite some differences in background housing and husbandry Specific factors that have been determined to be associated with stress in dogs living in confined environments include spatial restriction181923 extreme temperatures926 aversive interactions with kennel staff2627 lack of perceived control or the capacity to avoid or regulate exposure to aversive stimuli20ndash23 and limited access to positive human and conspecific social interactions182425 A recent study11 on the mental health of dogs formerly used as breeding stock in CBEs found severe and long-lasting adverse effects in dogs living in this type of environment offering evidence of the magnitude of stressors in CBEs

The stressors in the CBE environment may have acted at 2 stages of the developing puppiesrsquo lives the prenatal period and the first 8 weeks after birth A large body of research in humans and other animals has convincingly determined that prenatal stress (ie stress experienced by a pregnant female) causes alterations to the hypothalamic-pituitary-adrenal axis of the developing fetus that may manifest later in life as an impaired ability to cope with stress22 abnormal social behavior2829 and increased emotionality and fear-related behavior30 All of these outcomes are consistent with the differences detected in pet storendash versus NCB-obtained dogs (ie increased aggression fear of dogs and nonsocial stimuli and excitability) Substantial evidence in humans and other animals indicates that stressful experiences in early life may have extensive and enduring effects with strong correlations to later development of behavioral abnormalities and psychopathologic abnormalities31ndash35 In dogs Fox and Stelzner36 detected a short period at approximately 8 weeks of age when puppies are hypersensitive to distressing psychological or physical stimuli and during which a single unpleasant experience could result in long-term aversive or abnormal effects Transport-related stress was suggested by both Mugford4 and Gaultier et al6 to be a potentially critical factor in the early lives of puppies from CBEs as they are shipped to pet stores throughout North America Mugford4 Serpell and Jagoe2 and Bennett and Rohlf3 have each suggested that a reason for pet store and CBE puppies to have a high prevalence of behavioral problems later in life is inadequate early socialization In addition genetic influences may play a role in the differences between pet store and NCB dogs because a genetic basis for behavioral traits in dogs is consistent with findings observed in dogs of the present study including fear aggression emotional reactivity and nonspecific alterations in temperament and personality273738

The reported differences in the 2 groups of dogs in the present study could be attributable to a number of owner-related factors It is possible that people who buy puppies from pet shops may use different degrees or methods of training than people who buy puppies

from an NCB The importance of training in the development of problem behaviors was recently elucidated in the study3 of the relationship of potentially problematic behaviors with other variables The researchers found that for the 5 behavioral subscales the strongest predictor for scoring undesirably in 3 of the 5 subscales was the level of training the dog received The present study did not attempt to collect demographic or background information on the dog owners therefore the degree to which such factors may have contributed to the findings could not be assessed An additional owner-related consideration is that it is possible that people who buy puppies from pet stores simply report potentially problematic behaviors more readily than do others irrespective of the dogrsquos actual behavior

The data support the notion that dogs obtained as puppies from pet stores have substantial adverse behavioral differences compared with dogs obtained from NCBs Taken individually however the specific factors that differ between the 2 groups are not readily attributable to a single definitive explanation For example stranger-directed aggression may be attributable to inadequate socialization maltreatment by humans genetic factors and prenatal stress Taken collectively no single explanatory factor appears capable of accounting for the differences between the 2 groups For example although inadequate socialization may explain increased aggression the most prominent emotional consequence of insufficient socialization is fear2739 and whereas aggression toward humans (owners and unfamiliar people) was increased fear toward humans was not

There were a number of limitations to the present study The sample of dog owners was self-selected and therefore a potential source of bias The question in the C-BARQ regarding the source of the dogs did not define breeder leaving the participants to define the term for themselves Accordingly a breeder source could have indicated either type of NCB (hobby breeder or backyard breeder) and the level and type of care differ between the 2 types These differences are presumably minor in comparison to the differences between NCBs and CBEs It is also conceivable that the source of some dogs specified by the owner as breeder was a CBE however it is reasonable to conclude that there would be no overlap between breeder and pet store categories (ie no owner with a dog coming from a pet store would select breeder as a source and no owner with a dog coming from a breeder would select pet store as a source)

Results of the present study indicated that compared with dogs obtained as puppies from NCBs dogs obtained as puppies from pet stores had significantly greater aggression toward human family members unfamiliar people and other dogs fear of other dogs and nonsocial stimuli separation-related problems and urination and defecation problems in the home On almost all behavioral variables measured pet store dogs received less favorable scores than breeder-obtained dogs The diversity of behavioral differences between pet storendashobtained and breeder-obtained dogs suggests a multifactorial cause and accordingly a multifactorial approach to correction however the data did not permit determination of the specific contributory factors and the degree of influence they exerted In addition

1362 Scientific Reports JAVMA Vol 242 No 10 May 15 2013

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77

because we did not compare the 2 groups of dogs in 1

this study with other sources of dogs the results should not be interpreted as an endorsement of any particular source of dogs On the basis of these findings combined 1with earlier findings regarding pet storendashobtained dogs until the causes of the unfavorable differences detected 1in this group of dogs can be specifically identified and remedied we cannot recommend that puppies be ob 1

tained from pet stores 1

a Jagoe JA Behaviour problems in the domestic dog a retrospective and prospective study to identify factors influencing their development PhD thesis University of Cambridge Cambridge Eng 2land 1994

b Taylor K Senior Science Advisor Secretariat to the International Council for Animal Protection in Pharmaceutical Pro 2grames (ICAPPP) British Union for the Abolition of Vivisection (BUAV) 16a Crane Grove London England Personal communication 2011 2

c xtmixed Stata Statistical Software release 11 StataCorp College Station Tex

d xtmelogit Stata Statistical Software release 11 StataCorp College 2Station Tex

References 2

1 Fumarola AJ With best friends like us who needs enemies The phenomenon of the puppy mill the failure of legal regimes to 2manage it and the positive prospects of animal rights Buffalo Environ Law J 19996253ndash289

2 Serpell J Jagoe JA Early experience and the development of be 2havior In Serpell J ed The domestic dog its evolution behavior and interactions with people Cambridge England Cambridge 2University Press 199579ndash102

3 Bennett PC Rohlf VI Owner-companion dog interactions rela 2tionships between demographic variables potentially problematic behaviors training engagement and shared activities Appl Anim Behav Sci 200710265ndash84 2

4 Mugford RA Canine behavioral therapy In Serpell J ed The domestic dog its evolution behavior and interactions with people Cambridge England Cambridge University Press 1995139ndash152 3

5 Pierantoni L Albertini M Pirrone F Prevalence of owner- reported behaviors in dogs separated from the litter at two different ages Vet Rec 2011169468ndash474 3

6 Gaultier E Bonnafous L Vienet-Legue D et al Efficacy of dog-appeasing pheromone in reducing stress associated with social isolation in newly adopted puppies Vet Rec 200816373ndash80

7 Taylor K Mills DS A placebo-controlled study to investigate 3the effect of dog appeasing pheromone and other environmental and management factors on the reports of disturbance and house soiling during the night in recently adopted puppies (Cashynis familiaris) Appl Anim Behav Sci 2007105358ndash368

8 Hunte Corp Available at wwwhuntecorpcom Accessed Jun 5 3

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2011 9 USDA Final rules animal welfare 9 CFR parts 1 and 2 Avail 3

able at wwwnalusdagovawicpubsLegislatawafinshtml Accessed Jun 4 2011

10 USDA Animal welfare reports and electronic freedom of information frequent requests Available at wwwaphisusdagovanimal_ 3welfareefoia Accessed Feb 8 2012

11 McMillan FD Duffy DL Serpell JA Mental health of dogs formerly used as lsquobreeding stockrsquo in commercial breeding establish 3ments Appl Anim Behav Sci 201113586ndash94

12 Hsu Y Serpell JA Development and validation of a question 3naire for measuring behavior and temperament traits in pet dogs J Am Vet Med Assoc 20032231293ndash1300 3

13 Serpell JA Hsu Y Effects of breed sex and neuter status on trainability in dogs Anthrozoos 200518196ndash207 3

14 Duffy DL Hsu Y Serpell JA Breed differences in canine aggression Appl Anim Behav Sci 2008114441ndash460

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5 Van den Berg SM Heuven HCM Van den Berg L et al Evalushyation of the C-BARQ as a measure of stranger-directed agshygression in three common dog breeds Appl Anim Behav Sci 2010124136ndash141

6 Dohoo I Martin W Stryhn H Veterinary epidemiologic research 2nd ed Charlottetown PE Canada VER Inc 2009

7 StataCorp Stata 11 base reference manual College Station Tex Stata Press 2009242ndash278 306ndash355

8 Beerda B Schilder MB van Hooff JA et al Chronic stress in dogs subjected to social and spatial restriction I Behavioral reshysponses Physiol Behav 199966233ndash242

9 Beerda B Schilder MB Bernadina W et al Chronic stress in dogs subjected to social and spatial restriction II Hormonal and immunological response Physiol Behav 199966243ndash254

0 Stephen JM Ledger RA An audit of behavioral indicators of poor welfare in kenneled dogs in the United Kingdom J Appl Anim Welf Sci 2005879ndash96

1 Taylor KD Mills DS The effect of the kennel environment on canine welfare a critical review of experimental studies Anim Welf 200716435ndash447

2 Tuber DS Miller DD Caris KA et al Dogs in animal shelshyters problems suggestions and needed expertise Psychol Sci 199910379ndash386

3 Wells DL Graham L Hepper PG The influence of length of time in a rescue shelter on the behavior of kennelled dogs Anim Welf 200211317ndash325

4 Hughes HC Campbell S Kenney C The effects of cage size and pair housing on exercise of Beagle dogs Lab Anim Sci 198939302ndash305

5 Hubrecht RC A comparison of social and environmental enshyrichment methods for laboratory housed dogs Appl Anim Behav Sci 199337345ndash361

6 Morgan KN Tromborg CT Sources of stress in captivity Appl Anim Behav Sci 2007102262ndash302

7 Scott JP Fuller JL Genetics and the social behavior of the dog Chicago University of Chicago Press 1965

8 Braastad BO Effects of prenatal stress on behavior of offspring of laboratory and farmed mammals Appl Anim Behav Sci 199861159ndash180

9 Clarke AS Schneider ML Prenatal stress has long-term effects on behavioral responses to stress in juvenile rhesus monkeys Dev Psychobiol 199326293ndash304

0 Lehmann J Stoumlhr T Feldon J Long-term effects of prenatal stress experience and postnatal maternal separation on emotionality and attentional processes Behav Brain Res 2000107133ndash144

1 Edwards VJ Holden GW Felitti VJ et al Relationship between multiple forms of childhood maltreatment and adult mental health in community respondents results from the adverse childshyhood experiences study Am J Psychiatry 20031601453ndash1460

2 Ladd CO Huot RL Thrivikraman KV et al Long-term behavshyioral and neuroendocrine adaptations to adverse early experishyence In Mayer EA Saper CB eds Progress in brain research the biological basis for mind body interactions Amsterdam Elsevier 200081ndash103

3 Gunnar M Quevedo K The neurobiology of stress and developshyment Annu Rev Psychol 200758145ndash173

4 Tanapat P Hastings NB Rydel TA et al Exposure to fox odor inhibits cell proliferation in the hippocampus of adult rats via an adrenal hormone-dependent mechanism J Comp Neurol 2001437496ndash504

5 Dettling AC Feldon J Pryce CR Early deprivation and behavshyioral and physiological responses to separationnovelty in the marmoset Pharmacol Biochem Behav 200273259ndash269

6 Fox MW Stelzner D Behavioral effects of differential early exshyperience in the dog Anim Behav 196614273ndash281

7 Saetre P Strandberg E Sundgren PE et al The genetic contribushytion to canine personality Genes Brain Behav 20065240ndash248

8 Svartberg K Breed-typical behavior in dogsmdashhistorical remnants or recent constructs Appl Anim Behav Sci 200696293ndash313

9 Horwitz DF Neilson JC Blackwellrsquos five-minute veterinary conshysult clinical companionmdashcanine and feline behavior Ames Iowa Blackwell Publishing 2007

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ALL A

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JAVMA Vol 242 No 10 May 15 2013 Scientific Reports 1363

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79