Euthanasia of dogs at animal shelters is an important ethical issue in Israel, Australia, New Zealand, and many countries in Europe and North America. In the United States, euthanasia of dogs at animal shelters accounts for over one-third of all canine deaths and is the leading cause of death among domestic dogs.1,2 In 2006 and 2007, approximately 7,000 dogs were euthanized at Royal Society for the Prevention of Cruelty to Animals shelters in the state of Queensland, Australia, which represented 41% of all dogs and puppies entering these shelters.3 Unpublished data suggests that euthanasia rates are even higher in council (municipal)-run pounds.a
Behavioral problems are a common reason for the surrender and euthanasia of dogs. In a study4 of dogs admitted to 3 shelters in Victoria, Australia, 16% of relinquishers cited behavioral problems as a reason for relinquishment. However, a further one-third of relinquishers gave no reason and it is likely that behavior was also a factor in a proportion of these dogs.4 In studies conducted in the United Kingdom5 and Italy,6 31% and 39% of dogs, respectively, were relinquished for behavioral problems, and a US study7 found that behavioral problems were the most common reason for relinquishment. However, even these studies may have underestimated the actual proportion of dogs relinquished for behavior as behavioral problems are substantially underreported by owners.8 In a cross-sectional study8 in which owners relinquishing dogs to a shelter were asked to fill out a questionnaire, those who believed questionnaire responses were confidential reported owner-directed aggression and fear of strangers in their pets more frequently than did relinquishers who believed responses were not confidential. In the Victoria study,4 escaping, hyperactivity, and barking were the most common behavioral problems cited by relinquishers. This is similar to reports9,10 from US shelters in which hyperactivity and inappropriate chewing, elimination, and vocalization were the most frequently cited behavioral reasons for relinquishment. Importantly, of dogs euthanized at 3 shelters in Victoria, over half (54%) were euthanized for behavioral reasons, including aggression to people and animals, temperament (timid or untrustworthy), and other behavioral problems, including hyperactivity, inability to easily walk on a leash, barking, and escaping.4 Given that behavioral problems and temperament are major reasons for dog relinquishment and euthanasia in shelters,4,7,11 factors leading to poor behavior and temperament need to be identified and addressed.
There appears to be a critical socialization period for puppies, beginning at approximately 3 to 5 weeks of age and ending at approximately 9 to 14 weeks of age, with some disagreement in the literature.12,13 During this period, motor and perceptual development reaches maturity and the response to flee from strange stimuli is still not well developed.12,13 This balance of factors is thought to be critical for the formation of primary social relationships.12,13 For proper social relationships to develop, puppies need to not only interact with littermates and the bitch, but also be exposed to humans, novel situations, and environments during this period.14,15 Isolation during this critical period causes behavioral problems and decreases learning ability.15 A randomized controlled trial performed in the United Kingdom with 60 puppies found that those puppies receiving extra human socialization at 5 to 14 weeks of age were more approachable 6 to 11 months later than those that did not receive human socialization.16 Additionally, in a cohort study17 in which owners of 248 puppies adopted from shelters completed a questionnaire after they had been in the home for at least a week, a higher proportion of puppies that had attended puppy socialization classes before adoption were retained by the adopter. This indicates that early socialization with other dogs, unfamiliar humans and exposure to a variety of environments is associated with a decreased likelihood of behavioral problems later in life and is likely to reduce the chance of a dog being relinquished to a pound or shelter.
Therefore, inadequate socialization early in life appears to contribute to the number of dogs surrendered to shelters for behavioral reasons. However, no published studies have described socialization practices used by dog breeders. The purpose of the study reported here was to compare socialization practices used for litters bred by breeders registered in Queensland, Australia, with the CCC (currently called Dogs Queensland) and litters bred by nonregistered breeders advertising puppies for sale in a local newspaper.
Materials and Methods
Design—A retrospective cohort study was conducted to compare socialization practices used for litters bred by 40 registered breeders and those used for litters bred by 40 nonregistered breeders in Queensland via a questionnaire administered over the phone. Litters were selected by use of a 2-stage sample collection method. Registered breeders were randomly selected from the CCC website, and nonregistered breeders were randomly selected from a weekly advertising newspaper. The litter sold most recently by each breeder was then enrolled in the study.
The CCC in Queensland functions similarly to the American Kennel Club and provides a registry service for purebred dogs. Its website provides a list of breeders who have registered litters of puppies and their contact details.b Similar to the American Kennel Club, registration of puppies with the CCC is optional. The CCC also provides information to members on responsible dog ownership, including the keeping, welfare, breeding, selling, and disposing of dogs. It works with members to raise awareness of industry issues and improve industry standards.18
Selection criteria—For their litter to be enrolled in the study, registered breeders had to reside in Queensland, be registered with the CCC, and have had at least 1 bitch whelp in the previous 6 months. Nonregistered breeders had to reside in Queensland, not be registered with the CCC, and have advertised a litter < 12 weeks old for sale at the time they were selected.
Sampling frames, selection methods, and response rates—Based on the results of a pilot study, to obtain representative samples of registered and nonregistered breeders, individuals were selected from separate sampling frames. Nonregistered breeders were enrolled by selecting breeders from those offering puppies for sale through a local weekly private advertisement newspaperb on or between May 1 and June 25, 2008. To increase the probability that all puppies in the study litter were sold at the time the questionnaire was administered and hence all socialization practices by the breeder were complete for all puppies in the study litter, nonregistered breeders were contacted no sooner than 3 weeks after the advertisement appeared in the newspaper. Registered breeders were enrolled by selecting breeders from those listed on the CCC website.19
Complete lists of the population to be sampled (sampling frames) were developed separately for each group of breeders; these consisted of all breeders that, as far as could be ascertained before contact, met the selection criteria. Within each sampling frame, each breeder was assigned a number and a sample of breeders was then selected for contact by use of a computerized random number generator. Every breeder within each sampling frame had the same probability of being selected.
Selected breeders were asked questions about their most recently sold litter. Only 1 litter/breeder was enrolled. To ensure that no breeder was contacted more than once, each contact phone number was compared with a list of breeders that had already been contacted. Selected breeders were then contacted by telephone during daytime and evening hours. If the breeder was not contacted after 3 attempts, a replacement was randomly selected from the sampling frame and contact attempted. This was repeated until the required number of breeders of each type that met the selection criteria (40 of each type) agreed to answer the questionnaire. In total, 90 registered and 126 nonregistered breeders were selected to be contacted. Of these, 33 registered and 55 nonregistered breeders could not be reached in 3 attempts. Five registered breeders who were contacted did not meet the selection criterion of having at least 1 bitch whelp in the previous 6 months, and 12 registered and 31 nonregistered breeders who were contacted and met the selection criteria declined to answer the questionnaire. Thus, excluding breeders known to not meet the selection criteria, response rates were 47% (40/85) for registered breeders and 32% (40/126) for nonregistered breeders. The percentage of breeders who were contacted, met the selection criteria, and answered the questionnaire was 77% (40/52) for registered breeders and 56% (40/71) for nonregistered breeders.
Statistical power estimation—Before the study commenced, the statistical power for a study comparing the proportions of litters exposed to various socialization practices between 2 groups of 40 litters was calculated. This approach was used because sufficient resources existed to enroll no more than 80 litters and because statistical power for a fixed total sample size is usually maximized when group sizes are equal. Statistical power was estimated for detecting differences between 2 independent proportions by use of a formula for computing power for tests without continuity correction based on an asymptotic normal method20 and with α set at 0.05 (2 sided). Two-sided alternative hypotheses (ie, that the proportion of litters from registered breeders exposed to any particular socialization practice could be either higher or lower than that from nonregistered breeders) were appropriate as there was no a priori basis for specifying in advance that any difference in proportions could only occur in 1 direction for any socialization practice. This calculation showed that if the actual proportions differed between the 2 groups by ≥ 0.3, the study would have a statistical power > 0.78. Thus, a study that compared proportions of litters exposed to various socialization practices between 2 groups of 40 litters would be likely to detect significant differences between groups provided the actual proportions differed by at least moderate amounts. Software was used to make these estimates.21 This statistical power estimate should be viewed only as indicative because socialization practices were analyzed as ordinal data rather than being collapsed to binary variables as this approach assumes.
Questionnaire development and pilot study—To develop the questionnaire, a number of breeders and representatives from breed rescue groups were contacted to help the authors understand general socialization practices and identify key issues. Four breeders and 2 individuals involved in breed rescue groups were contacted by phone to discuss these issues before developing the questionnaire. The questionnaire consisted of 10 open-ended questions concerning the size and experience of the breeding operation and 32 questions in which the breeder was asked to identify how often they exposed their most recent litter to a particular stimulus. For this study, a run was an outdoor fenced area for confinement or exercise, and a whelping box was a small, open-topped box in which the bitch whelped and nursed the puppies. A kennel, as referred to in this study, was a small, portable or semiportable enclosure usually made of plastic or wood, with or without a closable door, that was typically kept outdoors or was a small enclosed area containing a dog bed (as is common in boarding kennels). The questionnaire took approximately 12 minutes to administer.
A pilot study was then performed involving 5 breeders randomly chosen from the advertising newspaper. It became evident during the choosing and contacting of these breeders that few litters advertised in the newspaper were being sold by breeders registered with the CCC. Thus, to select registered breeders, the study design was amended with the registered breeders cohort randomly selected from the CCC website and the pilot study extended to include 5 randomly selected registered breeders from this source. After revising the questionnaire, all breeders contacted in the pilot study were contacted again and the revised questionnaire administered so that they and their litters could be included in the main study.
The questionnairec was administered via telephone interview. Participants were informed by the interviewers that the study was being undertaken by the University of Queensland School of Veterinary Science to determine the socialization practices used by breeders. Questions focused on environmental variables thought to facilitate appropriate socialization of puppies that would minimize predisposing puppies to behavior problems identified in the literature as associated with relinquishment and euthanasia in shelters.4,7 All litter-specific questions were asked for the litter sold most recently at the time of the interview. The interviews were conducted by 2 interviewers. Each interviewer conducted approximately half the number of interviews for each category of breeder.
Data analysis—Proportions of litters that were conceived intentionally and locations in which the litter spent most of its time were compared between litters bred by registered and nonregistered breeders by use of the Fisher exact test. This test calculates the exact probability of observed data as extreme or more extreme than that actually observed should the null hypothesis be true for associations between pairs of categorical variables. This test was used to analyze these variables because it is not based on assumptions of large sample size and because there was no inherent order in categories of location in which the litter spent most of its time. For all other variables (minimum ages of puppies at sale or adoption and socialization practices), distributions were compared between litters bred by registered and non-registered breeders by use of the Mann-Whitney test with the improved normal approximation procedure of Hodges et al.22 The P value for this test is affected by differences in either the location or the shape of the observed distributions. This approach made use of the ranked nature of these data. Analyses were performed by use of a software program.21 Conclusions were based on associations where P < 0.05.
Results
Registered breeders who completed the questionnaire were predominantly small scale and reared a median of 3.5 litters every 2 years (range, 1 to 17 litters). For nonregistered breeders, the median total number of litters previously reared, not including the study litter, was 1 (range, 0 to 30 litters). At the time of interview, registered breeders had a median of 3.5 breeding bitches (range, 1 to 38 bitches), and for nonregistered breeders, the median number of breeding bitches was 1 (range, 1 to 6 bitches; P = 0.001). Minimum ages of puppies at sale or adoption by a new owner differed significantly (P = 0.001) between the 2 breeder types. Median minimum ages of puppies at the time of sale or adoption were 8 weeks for registered breeders (range, 5 to 10 weeks) and 7 weeks for nonregistered breeders (range, 4 to 10 weeks). Thirty percent (12/40) of litters bred by nonregistered breeders were of mixed breeding.
Proportions of litters that were conceived by intentional mating differed significantly (P = 0.007) between registered and nonregistered breeders. Nearly all (39/40 [98%]) study litters bred by registered breeders were conceived through an intentional mating, whereas 75% (30/40) of study litters bred by nonregistered breeders were intentional.
Frequencies of exposure to other animals for litters bred by registered and nonregistered breeders were summarized (Table 1). Litters bred by registered breeders were exposed more frequently to unfamiliar dogs that were not part of the normal household. They were also exposed more frequently than were litters bred by non-registered breeders to dog breeds that were different from the bitch and sire's breed and to adult dogs that were not the bitch or sire but were part of the household.
Comparison of frequencies of exposure to other animals between litters of dogs bred by CCC-registered breeders (n = 40) versus litters of nonregistered breeders (40) in Queensland, Australia.
| No. (%) of litters | ||||
|---|---|---|---|---|
| Stimulus | Frequency of exposure | Registered breeders | Nonregistered breeders | P value |
| Unfamiliar dogs not in household | Daily | 5(12.5) | 1 (2.5) | 0.033 |
| Several times per week | 2 (5.0) | 2 (5.0) | ||
| Weekly | 4(10.0) | 0 (0.0) | ||
| Occasionally | 5(12.5) | 5(12.5) | ||
| Never | 24 (60.0) | 32 (80.0) | ||
| Dogs of breeds other than the bitch's or sire's breed | Daily | 10 (25.0) | 5 (12.5) | 0.038 |
| Several times per week | 3 (7.5) | 3 (7.5) | ||
| Weekly | 3 (7.7) | 0 (0.0) | ||
| Occasionally | 7 (17.5) | 6 (15.0) | ||
| Never | 17 (42.5) | 26 (65.0) | ||
| Cats | Daily | 8 (20.0) | 10 (25.0) | 0.208 |
| Several times per week | 0 (0.0) | 2 (5.0) | ||
| Weekly | 0 (0.0) | 0 (0.0) | ||
| Occasionally | 1 (2.5) | 3 (7.5) | ||
| Never | 31 (77.5) | 25 (62.5) | ||
| Livestock | Daily | 10 (25) | 7 (17.5) | 0.428 |
| Several times per week | 2 (5.0) | 2 (5.0) | ||
| Weekly | 1 (2.5) | 0 (0.0) | ||
| Occasionally | 1 (2.5) | 2 (5.0) | ||
| Never | 26 (65.0) | 29 (72.5) | ||
| Other pets | Daily | 9 (22.5) | 5 (12.5) | 0.647 |
| Several times per week | 0 (0.0) | 2 (5.0) | ||
| Weekly | 0 (0.0) | 0 (0.0) | ||
| Occasionally | 0 (0.0) | 1 (2.5) | ||
| Never | 31 (77.5) | 32 (80.0) | ||
| Adult dogs in household other than the bitch or sire | Daily | 34 (85.0) | 12 (30.0) | < 0.001 |
| Several times per week | 0 (0.0) | 0 (0.0) | ||
| Weekly | 1 (2.5) | 0 (0.0) | ||
| Occasionally | 1 (2.5) | 0 (0.0) | ||
| Never | 4(10.0) | 28 (70.0) | ||
Frequencies of exposure to environmental stimuli for litters bred by registered and nonregistered breeders were summarized (Table 2). Litters bred by registered breeders were exposed more frequently to people wearing hats and sunglasses and were walked on a leash and taken for car rides more frequently. Litters bred by registered breeders were also exposed more frequently to loud noises, such as lawn mowers, telephones, and vacuum cleaners. Locations in which litters spent most of their time differed between registered and nonregistered breeders. Most litters bred by registered breeders spent most of their time either in the home (48% [19/40] of litters) or in a kennel (30% [12/40]), whereas most litters bred by unregistered breeders spent most of their time in a run (33% [13/40] of litters) or a backyard (33% [13/40]). Importantly, whereas 48% (19/40) of litters from registered breeders spent most of their time in the home, only 8% (3/40) of litters bred by nonregistered breeders did so. However, litters bred by registered breeders were also more likely to spend some time in a run on a daily basis than were litters from nonregistered breeders.
Comparison of frequencies of exposure to environmental stimuli between litters of dogs bred by CCC-registered breeders (n = 40) versus litters of nonregistered breeders (40).
| No. (%) of litters | ||||
|---|---|---|---|---|
| Stimulus | Frequency of exposure | Registered breeders | Nonregistered breeders | P value |
| People wearing hats and sunglasses | Daily | 26 (65.0) | 18 (45.0) | 0.043 |
| Several times per week | 5 (12.5) | 9 (22.5) | ||
| Weekly | 5 (12.5) | 1 (2.5) | ||
| Occasionally | 2 (5.0) | 1 (2.5) | ||
| Never | 2 (5.0) | 11 (27.5) | ||
| People carrying walking sticks or umbrellas | Daily | 8 (20.0) | 9 (22.5) | 0.682 |
| Several times per week | 2 (5.0) | 2 (5.0) | ||
| Weekly | 2 (5.0) | 2 (5.0) | ||
| Occasionally | 10 (25.0) | 11 (27.5) | ||
| Never | 18 (45.0) | 16 (40.0) | ||
| Baby carriage | Daily | 2 (5.0) | 6 (15.0) | 0.667 |
| Several times per week | 3 (7.5) | 1 (2.5) | ||
| Weekly | 3 (7.5) | 2 (5.0) | ||
| Occasionally | 1 (2.5) | 1 (2.5) | ||
| Never | 31 (77.5) | 30 (75.0) | ||
| Bicycles | Daily | 5 (12.5) | 6 (15.0) | 0.037 |
| Several times per week | 3 (7.5) | 10 (25.0) | ||
| Weekly | 1 (2.5) | 1 (2.5) | ||
| Occasionally | 5 (12.5) | 7 (17.5) | ||
| Never | 26 (65.0) | 16 (40.0) | ||
| Motorcycles | Daily | 4 (10.0) | 5 (12.5) | 0.847 |
| Several times per week | 2 (5.0) | 3 (7.5) | ||
| Weekly | 5 (12.5) | 0 (0.0) | ||
| Occasionally | 3 (7.5) | 5 (12.5) | ||
| Never | 26 (65.0) | 27 (67.5) | ||
| Car rides | Daily | 0 (0.0) | 0 (0.0) | 0.006 |
| Several times per week | 6 (15.0) | 1 (2.5) | ||
| Weekly | 7 (17.5) | 3 (7.5) | ||
| Occasionally | 25 (62.5) | 30 (75.0) | ||
| Never | 2 (5.0) | 6 (15.0) | ||
| Heavy traffic | Daily | 7 (17.5) | 10 (25.0) | 0.670 |
| Several times per week | 4 (10.0) | 0 (0.0) | ||
| Weekly | 3 (7.5) | 2 (5.0) | ||
| Occasionally | 13 (32.5) | 12 (30.0) | ||
| Never | 13 (32.5) | 16 (40.0) | ||
| Kept in kennel | Daily | 17 (42.5) | 17 (42.5) | 0.894 |
| Several times per week | 1 (2.5) | 0 (0.0) | ||
| Weekly | 0 (0.0) | 0 (0.0) | ||
| Occasionally | 0 (0.0) | 0 (0.0) | ||
| Never | 22 (55.0) | 23 (57.5) | ||
| Kept in run | Daily | 17 (42.5) | 7 (17.5) | 0.009 |
| Several times per week | 1 (2.5) | 0 (0.0) | ||
| Weekly | 0 (0.0) | 0 (0.0) | ||
| Occasionally | 0 (0.0) | 0 (0.0) | ||
| Never | 22 (55.0) | 33 (82.5) | ||
| Kept in the backyard | Daily | 22 (55.0) | 27 (67.5) | 0.293 |
| Several times per week | 1 (2.5) | 0 (0.0) | ||
| Weekly | 0 (0.0) | 0 (0.0) | ||
| Occasionally | 0 (0.0) | 0 (0.0) | ||
| Never | 17 (42.5) | 13 (32.5) | ||
| Kept in the home | Daily | 30 (75.0) | 23 (57.5) | 0.162 |
| Several times per week | 1 (2.5) | 4 (10.0) | ||
| Weekly | 1 (2.5) | 0 (0.0) | ||
| Occasionally | 1 (2.5) | 5 (12.5) | ||
| Never | 7 (17.5) | 8 (20.0) | ||
| Kept mostly in kennel, run, backyard, or home | Kennel | 12 (30.0) | 11 (27.5) | < 0.001 |
| Run | 6 (15.0) | 13 (32.5) | ||
| Backyard | 3 (7.5) | 13 (32.5) | ||
| Home | 19 (47.5) | 3 (7.5) | ||
| Kept in whelping box | Daily | 22 (55.0) | 12 (30.0) | 0.184 |
| Several times per week | 0 (0.0) | 2 (5.0) | ||
| Weekly | 0 (0.0) | 0 (0.0) | ||
| Occasionally | 2 (5.0) | 9 (22.5) | ||
| Never | 16 (40.0) | 17 (42.5) | ||
| Walked on a leash | Daily | 8 (20.0) | 1 (2.5) | < 0.001 |
| Several times per week | 6 (15.0) | 6 (15.0) | ||
| Weekly | 3 (7.5) | 1 (2.5) | ||
| Occasionally | 9 (22.5) | 1 (2.5) | ||
| Never | 14 (35.0) | 31 (77.5) | ||
| Walked up and down stairs | Daily | 11 (27.5) | 12 (30) | 0.572 |
| Several times per week | 1 (2.5) | 2 (5.0) | ||
| Weekly | 0 (0.0) | 1 (2.5) | ||
| Occasionally | 1 (2.5) | 1 (2.5) | ||
| Never | 27 (67.5) | 24 (60.0) | ||
| Telephone noise | Daily | 37 (92.5) | 28 (70.0) | 0.012 |
| Several times per week | 0 (0.0) | 1 (2.5) | ||
| Weekly | 0 (0.0) | 2 (5.0) | ||
| Occasionally | 1 (2.5) | 3 (7.5) | ||
| Never | 2 (5.0) | 6 (15.0) | ||
| Washing machine noise | Daily | 7 (17.5) | 6 (15.0) | 0.099 |
| Several times per week | 18 (45.0) | 11 (27.5) | ||
| Weekly | 5 (12.5) | 6 (15.0) | ||
| Occasionally | 2 (5.0) | 2 (5.0) | ||
| Never | 8 (20.0) | 15 (37.5) | ||
| Lawn mower noise | Daily | 2 (5.0) | 1 (2.5) | 0.014 |
| Several times per week | 0 (0.0) | 0 (0.0) | ||
| Weekly | 11 (27.5) | 3 (7.5) | ||
| Occasionally | 16 (40.0) | 17 (42.5) | ||
| Never | 11 (27.5) | 19 (47.5) | ||
| Vacuum cleaner noise | Daily | 5 (12.5) | 4 (10.0) | 0.011 |
| Several times per week | 15 (37.5) | 2 (5.0) | ||
| Weekly | 9 (22.5) | 15 (37.5) | ||
| Occasionally | 3 (7.5) | 6 (15.0) | ||
| Never | 8 (20.0) | 13 (32.5) | ||
Frequencies of exposure to people for litters bred by registered and nonregistered breeders were summarized (Table 3). There were no significant differences between breeder groups in frequencies of exposure of litters of puppies to babies, children, teenagers, elderly people, men, and women. However, litters from non-registered breeders were exposed more frequently to smokers than were those from registered breeders.
Comparison of frequencies of exposure to people of various types between litters of dogs bred by CCC-registered breeders (n = 40) versus litters of nonregistered breeders (40).
| No. (%) of litters | ||||
|---|---|---|---|---|
| Stimulus | Frequency of exposure | Registered breeders | Nonregistered breeders | P value |
| Babies | Daily | 3 (7.5) | 2 (5.0) | 0.822 |
| Several times per week | 2 (5.0) | 4 (10.0) | ||
| Weekly | 2 (5.0) | 1 (2.5) | ||
| Occasionally | 3 (7.5) | 2 (5.0) | ||
| Never | 30 (75.0) | 31 (77.5) | ||
| Children | Daily | 9 (22.5) | 13 (32.5) | 0.398 |
| Several times per week | 8 (20.0) | 8 (20.0) | ||
| Weekly | 6 (15.0) | 4 (10.0) | ||
| Occasionally | 10 (25.0) | 9 (22.5) | ||
| Never | 7 (17.5) | 6 (15.0) | ||
| Teenagers | Daily | 5 (12.5) | 13 (32.5) | 0.903 |
| Several times per week | 4 (10.0) | 1 (2.5) | ||
| Weekly | 8 (20.0) | 2 (5.0) | ||
| Occasionally | 7 (17.5) | 4 (10.0) | ||
| Never | 16 (40.0) | 20 (50.0) | ||
| Elderly people | Daily | 16 (40.0) | 11 (27.5) | 0.186 |
| Several times per week | 1 (2.5) | 3 (7.5) | ||
| Weekly | 3 (7.5) | 2 (5.0) | ||
| Occasionally | 8 (20.0) | 6 (15.0) | ||
| Never | 12 (30.0) | 18 (45.0) | ||
| Smokers | Daily | 5 (12.5) | 12 (30.0) | 0.006 |
| Several times per week | 0 (0.0) | 4 (10.0) | ||
| Weekly | 3 (7.5) | 1 (2.5) | ||
| Occasionally | 3 (7.5) | 6 (15.0) | ||
| Never | 29 (72.5) | 17 (42.5) | ||
| Women not in the household | Daily | 6 (15.0) | 0 (0.0) | 0.283 |
| Several times per week | 9 (22.5) | 20 (50.0) | ||
| Weekly | 13 (32.5) | 2 (5.0) | ||
| Occasionally | 12 (30.0) | 11 (27.5) | ||
| Never | 0 (0.0) | 7 (17.5) | ||
| Men not in the household | Daily | 3 (7.5) | 0 (0.0) | 0.587 |
| Several times per week | 10 (25.0) | 18 (45.0) | ||
| Weekly | 13 (27.5) | 4 (10.0) | ||
| Occasionally | 12 (30.0) | 10 (25.0) | ||
| Never | 2 (5.0) | 8 (20.0) | ||
Discussion
The present study found that litters bred by small-scale registered breeders had more social interactions of the types investigated than those of small-scale non-registered breeders. Litters bred by registered breeders are more frequently socialized with unfamiliar adult dogs and exposed more frequently to varied environmental stimuli and people of different appearances. The finding that nonregistered breeders provide fewer early social interactions, compared with registered breeders, is important because inadequate early socialization increases risks of subsequent behavioral problems, and many unwanted pets are surrendered and euthanized as a result of behavioral reasons, including poor sociability with humans.7,10
This study was limited to analyzing the socialization practices investigated in the interview and did not encompass the entire scope of possible socialization practices used by breeders. The questionnaire focused on variables that would indicate exposure to people, other animals, and a range of experiences that would be encountered by a puppy after sale or adoption. For proper social relationships to develop, it is reported that puppies need exposure to humans, novel situations, and environments and that isolation causes behavioral problems and decreased learning ability.14,15,23 The questionnaire particularly focused on exposure to humans in a variety of environments and exposure to other animals, including dogs, because aggression to people and other animals is a major reason for euthanasia.4
Litters bred by registered breeders were socialized more frequently with adult dogs other than the bitch or sire probably because there were multiple breeding bitches in the household, compared with only a single bitch in the households of most nonregistered breeders. Registered breeders also exposed their puppies to unfamiliar dogs and dogs of different breeds more frequently. Puppies that do not have an opportunity to interact with other dogs during the critical socialization period may later develop undesirable behavior, such as hyper-activity, aggression, and fear toward other dogs.14,15,23,24 Aggression toward other dogs is an important cause of euthanasia. In a study4 of dogs in 3 shelters in Victoria, Australia, 25% of dogs euthanized were done so for aggression. Of these, 38% were euthanized for aggression toward other dogs.4
Litters bred by registered breeders were exposed more frequently to people wearing hats and sunglasses. Although there was no difference between breeder groups in frequency of exposure of litters to people of different ages, it is likely the duration of each exposure was longer for litters from registered breeders because they spent significantly more time inside the home than did litters from unregistered breeders. Puppies not exposed to people of different appearances and age groups have been reported to be at increased risk of unwanted behavior later in life.14,15,23,24 Aversion to people of strange appearance, aggression toward strangers, excessive barking, and fear on walks are examples of problem behaviors of dogs that have been poorly socialized with people.23 Furthermore, unless socialized with people before 14 weeks of age, the withdrawal response to humans can be so great that a puppy is at high risk of becoming untrainable.13 The study4 completed in Victoria found that of dogs euthanized for aggression, 57% were euthanized for aggression toward humans. This included dogs with a history of aggression and those that were aggressive on testing.4
A higher proportion of litters bred by nonregistered breeders spent most of their time in the backyard. In contrast, almost half (47.5%) of the litters bred by registered breeders spent most of their time in the home, compared with only 7.5% of litters bred by nonregistered breeders. Spending more time inside the home (as distinct from in the backyard) would be expected to increase interaction between puppies and humans and to expose puppies to more varied stimuli, including noises and odors, similar to what they would subsequently encounter as a newly acquired pet that spends a portion of its life inside the home. This is likely to be why litters bred by registered breeders were more likely to be exposed to a variety of normal household noises, such as those produced by vacuum cleaners and telephones. These breeders also took their puppies on car rides more frequently.
Although not a significant difference, a larger percentage (50% vs 33%) of litters bred by registered breeders spent time on a daily basis in a whelping box. Confinement training has been shown to be an effective tool for housetraining pets, which could in turn reduce unwanted behavior such as inappropriate elimination, destructiveness, and separation anxiety.25 Because inappropriate elimination posed the greatest risk for relinquishment of any behavior and results in a higher risk for relinquishment than even aggression,11 successful housetraining is essential for protecting puppies from subsequent relinquishment.
Registered breeders walked their puppies on a leash more frequently. Many dogs are aggressive and excessively exuberant during leash walking.24 Early exposure to leash walking may reduce the likelihood of subsequent problem behaviors. Hyperactivity or excessive exuberance, poor trainability, and aggression are common reasons why dogs are relinquished to and euthanized at shelters.4–7,9–11
Registered breeders started selling or adopting out their puppies at older ages (mean, 8 weeks) than did non-registered breeders (mean, 7 weeks). Interaction between littermates and the bitch influence a puppy's trainability and sociability to humans and other dogs.26 According to Wilsson,26 these interactions peak when the puppy is 7 weeks old. Early separation of puppies from the bitch and their littermates can lead to the development of problem behavior and subsequent relinquishment.13,26
Twenty-five percent of litters bred by nonregistered breeders were the result of unintentional mating, compared with only 2% of those from registered breeders. It is possible that puppies from unplanned litters are less likely to be sold or adopted and more likely to be relinquished to shelters or pounds. There are no reported studies of whether puppies from unplanned litters are at greater risk of relinquishment than puppies from planned litters. However, puppies from unplanned litters might be sold for lower amounts or given gratis more often and puppies acquired at low or no cost are reportedly at greater risk of relinquishment.10,11 Therefore, strategies to reduce the incidence of unintentional pregnancies might reduce the numbers of dogs entering shelters.
Many nonregistered breeders in this study were first-time breeders and thus had little previous experience raising a litter of puppies, compared with registered breeders, most of whom had raised multiple previous litters. It is possible that this lack of experience contributed to the decreased frequency of socialization exposures identified in the present study.
A potential limitation of this study was the fact that recall time was in some cases longer for registered breeders than for nonregistered breeders. Because of time and resource constraints of the study, to facilitate recruitment of equal numbers of registered and non-registered breeders, the selection criteria allowed enrollment of registered breeders that had at least 1 bitch whelp in the previous 6 months. Therefore, recall time for registered breeders was up to 6 months, whereas recall time for nonregistered breeders was approximately 3 weeks, as nonregistered breeders were contacted 3 weeks after their advertisement appeared in the newspaper. Thus, it is possible that some registered breeders were recalling their perceived general socialization practices rather than practices specifically used for the most recent litter whelped. This would not result in recall bias if socialization practices by each breeder were consistent across litters but may have been a source of bias if practices varied among litters bred by the same breeder. Another potential limitation of this study was that the questionnaire was not validated and the repeatability of responses to the study questions was not assessed. However, misclassification errors were probably minimal as most questions were objective. Additionally, interviewers were not blinded to the status of the breeder. This was not possible because the interviewers needed to determine whether each breeder interviewed was eligible to be enrolled in the study. However, as questions were objective, there was limited potential for the interviewers to misinterpret or influence responses. A notable strength of this study was the random selection of breeders from complete sampling frames. Random selection of research subjects is an unusual feature of cohort studies and would be expected to reduce selection bias. However, there was potential for nonresponse bias as response rates were low to moderate and were higher for registered breeders than for nonregistered breeders. A bias would occur if nonresponding breeders exposed their litters to socialization stimuli less often than did respondents. The major reason for non-response was inability to make contact with selected breeders, but nonresponse was also due to some breeders declining to answer the questionnaire.
Because most registered breeders interviewed were small scale (1 to 6 bitches), it was not possible to determine whether practices differed between small- and large-scale registered breeders. Large-scale breeders would commonly have multiple litters whelping during the same period. It is possible that these breeders would provide their puppies with less frequent exposure to socialization stimuli because of their scale. Additionally, this study only addressed the frequency of exposure of puppies to various stimuli and did not investigate the nature or duration of these exposures. Further study is needed to determine whether the quality of exposures also differs among different registered breeder groups.
In conclusion, litters from small-scale registered breeders receive greater frequency of social interactions, compared with litters from nonregistered breeders. Small-scale registered breeders have more experience raising puppies, and their litters are socialized more frequently with adult dogs and people of different appearances and are exposed more frequently to varied environmental stimuli, compared with those of nonregistered breeders. We recommend that people purchasing puppies from nonregistered breeders focus on socializing their puppies between purchase and 14 weeks of age as this may be a deficit in the rearing practices of these types of breeders. Additional research is required to determine whether puppies from nonregistered breeders are at increased risk for behavioral problems and are more likely to be relinquished to animal shelters or euthanized, relative to puppies from registered breeders.
ABBREVIATION
| CCC | Canine Control Council |
Verrinder J, Animal Welfare League of Queensland, Helensvale, QLD, Australia: Personal communication, 2008.
Trading Post, Queensland Edition, BigPond, Melbourne, VIC, Australia.
Copies of the revised questionnaire are available upon request from the corresponding author.
References
1. Olson P, Moulton C, Nett T, et al. Pet overpopulation: a challenge for companion animal veterinarians in the 1990s. J Am Vet Med Assoc 1991; 198:1151–1152.
2. Patronek GJ, Glickman LT, Moyer MR. Population dynamics and the risk of euthanasia of dogs in an animal shelter. Anthrozoos 1995; 8:31–43.
3. RSPCA Queensland Inc. RSPCA Queensland annual report 2006–2007!. Available at: www.rspcaqld.org.au/aboutus/RSPCA-Qld-Annual-Report-06-07.pdf. Accessed Sep 17, 2008.
4. Marston LC, Bennett PC, Coleman GJ. What happens to shelter dogs? An analysis of data for 1 year from three Australian shelters. Appl Anim Welf Sci 2004; 7:27–47
5. Wells DL, Hepper PG. Prevalence of behavior problems reported by owners of dogs purchased from an animal rescue shelter. Appl Anim Behav Sci 2000; 69:55–65.
6. Mondelli F, Previde EP, Verga M, et al. The bond that never developed: adoption and relinquishment of dogs in a rescue shelter. J Appl Anim Welf Sci 2004; 7:253–266.
7. DiGiacomo N, Arluke A, Patronek G. Surrendering pets to shelters: the relinquisher's perspective. Anthrozoos 1998; 11:41–51.
8. Segurson SA, Serpell JA, Hart BL. Evaluation of a behavioral assessment questionnaire for use in the characterization of behavioral problems of dogs relinquished to animal shelters. J Am Vet Med Assoc 2005; 227:1755–1761.
9. Miller D, Staats S, Partlo C, et al. Factors associated with decision to surrender a pet to an animal shelter. J Am Vet Med Assoc 1996; 209:738–742.
10. Salmon N, New J, Scarlett M, et al. Human and animal factors related to the relinquishment of dogs and cats in 12 selected animal shelters in the United States. J Appl Anim Welf Sci 1998; 1:207–226.
11. Patronek GJ, Glickman LT, Beck AM, et al. Risk factors for relinquishment of dogs to an animal shelter. J Am Vet Med Assoc 1996; 209:572–581.
12. Scott JP. The process of primary socialization in canine and human infants. Monogr Soc Res Child Dev 1963; 28:1–47.
13. Freedman DG, King JA, Orville E. Critical period in the social development of dogs. Science 1961; 133:1016–1017.
14. Seksel K. Preventing behavior problems in puppies and kittens. Vet Clin North Am Small Anim Pract 2008; 38:971–982.
15. Seksel K. Puppy socialization classes. Vet Clin North Am Small Anim Pract 1997; 27:465–477.
16. Hubrecht RC. Enrichment in puppyhood and its effects on later behavior of dogs. Lab Anim Sci 1995; 45:70–75.
17. Duxbury MM, Jackson JA, Line SW, et al. Evaluation of association between retention in the home and attendance at puppy socialization classes. J Am Vet Med Assoc 2003; 223:61–66.
18. Canine Control Council of Queensland. CCC(Q) rule book and code of ethics!. March 2010. Available at: www.cccq.org.au/media/scripts/DownloadHandler.ashx?did=471. Accessed May 1, 2010.
19. Canine Control Council of Queensland. Available at: www.cccq.org.au/breeders.html. Accessed Jul 6, 2008.
20. Sahai H, Khurshid A. Formulae and tables for the determination of sample sizes and power in clinical trials for testing differences in proportions for the two-sample design: a review. Stat Med 1996; 15:1–21
21. Abramson JH. WINPEPI (PEPI-for-Windows): computer programs for epidemiologists. Epidemiol Perspect Innov 2004; 1:6.
22. Hodges JH, Ramsey PH, Wechsler S. Improved significance probabilities of the Wilcoxon test. J Educ Stat 1990; 15:249–265
23. Pierantoni L, Verga M. Behavioral consequences of premature maternal separation and lack of stimulation during the socialization period in dogs. J Vet Behav 2007; 2:84–85.
24. Haug LI. Canine aggression towards unfamiliar people and dogs. Vet Clin North Am Small Anim Pract 2008; 38:1023–1041.
25. Vollmer PJ. Puppy rearing 4: crate-training the pup. Vet Med Small Anim Clin 1978; 73:1265–1267.
26. Wilsson E. The social interaction between mother and offspring during weaning in German Shepherd Dogs: individual differences between mothers and their effects on offspring. Appl Anim Behav Sci 1984; 13:101–112.
