According to Scott and Fuller (1), the juvenile period in dogs runs from ~12 weeks (the postulated end of the socialization period) until 6 months of age or later, corresponding to the onset of sexual maturation (i.e., puberty). Extensive studies in rodents and both human and non-human primates have demonstrated that changes in circulating gonadal hormones during the adolescent period have dramatic effects on brain development and behavior in mammals (2, 3). Despite the likelihood of similar developmental influences in adolescent dogs (between ~6 months and 1–2 years of age depending on the individual and breed), this period is probably the most poorly studied in terms of its effects on adult behavior (4). Anecdotal evidence certainly suggests that experiences during the juvenile and adolescent periods appear exert long-term effects on behavior in dogs (5–8), and one recent study of military working dogs found a positive association between dogs’ overall scores for working ability and the amount of time they were left at home alone during this period (9). In rodents, exposure to enriched environments around puberty has been found to erase the negative effects of early life stress on the development of the HPA axis (10), but whether similar effects occur in dogs is currently unknown.

Purpose-bred guide dogs provide a useful model for studying canine behavioral development during this period for several reasons. First, they usually comprise a relatively small number of different breed types – typically Labrador retriever, golden retriever, German Shepherd dog (GSD), and Labrador × golden retriever crosses – and this enables both within-breed and across-breed comparisons. Second, these dogs remain sexually intact until around 14–18 months of age so the potentially confounding effects of the loss of gonadal hormones on brain development and behavior due to surgical sterilization are effectively eliminated. Third, up to the age of 7–9 weeks, the puppies produced within any given organization will experience similar and relatively consistent early rearing environments, thus helping to reduce the effects of differential environmental influences occurring during early development. Finally, from roughly 2 to 14 months of age, guide dog puppies are reared in the households of volunteer puppy raisers (i.e., individuals and families who foster guide dog puppies) where they are exposed to variable environments, thereby providing an opportunity to explore the possible effects of this variability on their behavioral development during the juvenile and adolescent periods. Here, we present findings based on behavioral data collected from puppy raisers associated with a single guide dog organization when the dogs were 6 and 12 months of age, respectively. In addition to exploring maturational changes in behavior in dogs between 6 and 12 months (i.e., assumed to represent juvenile and adolescent dogs, respectively), we also investigate associations between behavioral outcomes at 12 months of age, and during subsequent training, and antecedent environmental factors and events occurring during the juvenile and adolescent periods.

This analysis of guide dog development has been able to partially isolate the effects of the post-socialization rearing environment from those arising from events and exposures occurring during the earlier prenatal, neonatal, and primary socialization periods. Although the conclusions that can be drawn from retrospective reports are inevitably somewhat limited, the findings support the view that certain events and experiences occurring during the juvenile and adolescent periods are predictive of behavioral outcomes at 12 months of age, and that different breeds appear to respond differently to these experiences. Whether such associations are restricted to particular sensitive periods, or are equally likely to occur at any time throughout this stage of development, is unknown. However, the current analysis of maturational changes suggests that some dogs are predisposed to develop aggressive reactions to unfamiliar individuals between roughly 6 and 12 months of age, and that this predisposition is stronger in the German Shepherd breed than in the other three breed types investigated. This finding is of interest in light of anecdotal reports of a phase of heightened sensitivity to territorial stimuli in wolves at around 4–5 months age [see Ref. (6–8)], and also indicates that this onset of defensive behavior is not necessarily associated with a corresponding increase in fear of strangers. This implies that the aggressive element of defensive/territorial behavior develops separately from the fearful component, and suggests that such fears may become established earlier in life. Since owner-directed aggression decreases in all breeds over the same period, the findings further suggest that the rise in stranger-directed aggression in German Shepherds is not due to an overall increase in aggressiveness, but rather a specific response to unfamiliar persons. These results also reinforce the view that it is the interaction between a dog’s genetic background and its developmental environment that ultimately determines the adult behavioral phenotype.

With respect to developmental effects of specific events and exposures during this period, the findings illustrate the important role that the puppy-raiser’s puppy-rearing experience plays in determining behavioral outcomes, as well as the value of social exposure to other dogs in the household. Both of these variables are potentially modifiable either through education, in the case of experience, or through the deliberate recruitment of puppy raisers from among existing experienced dog owners, and such efforts or interventions would be likely to have a significant positive impact on the performance of future working dogs, especially for those breeds that are predisposed to developing problems.

The results also draw attention to the apparent sensitivity of dogs at this age to the effects of traumatic events or experiences, such as being frightened by a person, or being threatened or attacked by another dog. Such findings reinforce the view that puppies and young dogs are sensitive to aversive social encounters long after the ostensible end of the socialization period (i.e., 12 weeks), and that such encounters may have long-term negative consequences for behavior. Unfortunately, because of the correlational nature of these outcomes, it is not possible to determine whether these dogs became more fearful and/or aggressive as a direct consequence of their experiences or if they were more likely to be traumatized by an aversive encounter due to a pre-existing disposition toward fearfulness.

While some of the current results are unsurprising – for example, the reduced scores for the C-BARQ variables dog-directed fear and dog-directed aggression among puppies reared with other dogs – others are less easy to interpret. The reduction in “owner-directed aggression” in multi-dog households could perhaps be attributed to puppies developing enhanced social skills as a consequence of entering households at the bottom of established hierarchies. A study of pet dogs in Taiwan also found lower rates of owner-directed aggression among dogs living in multi-dog households (13), and an early study of guide dog puppies found that those reared in homes with other dogs were less distracted by other unfamiliar dogs when tested on walks at 6 and 12 months of age (14). By contrast, an Australian study of GSDs found that the presence of another dog in the household had a deleterious effect on dogs’ scores on tests of fearfulness, social attraction and “dominance” (15), while a recent study of guide dog puppies in the UK found a positive association between puppies’ ratings for energy level and distractibility and the number of dogs in the puppy-raising household (16).

With respect to puppy-raiser experience, these results are in agreement with those of previous studies that found that pet dogs belonging to first-time dog owners were more likely to display owner-directed aggression than those of more experienced owners (17, 18). One interpretation of such findings is that dog owners learn from experience how to prevent the development of some canine behavior problems, and that they get better at doing this with each successive dog owned. Similar effects may also account for the reduced energy and distractibility ratings of puppies reared by more experienced “puppy walkers” in a recent UK study of guide dogs (16). It is also possible that puppy-raising experience enhances owners’/handlers’ ability to “read” and react to canine emotions. Previous research has shown, for example, that increasing levels of experience with dogs is associated with improved human ability to recognize canine emotions, such as fear (19).

Most previous studies of canine behavioral development have tended to focus exclusively on the traditional 3- to 12-week socialization period, and this has perhaps discouraged investigators from exploring the possible consequences of later exposure to biologically relevant events and stimuli. Further investigations that emphasize the precise timing and quality of experiences within this developmental period would be likely to yield valuable information regarding appropriate husbandry practices for dogs of this age.

The study was approved by the Privately-owned Animals Subcommittee of the University of Pennsylvania Institutional Animal Care and Use Committee. The guide dogs and the survey data that were used in this study were owned by The Seeing Eye, Inc., Morristown, NJ, USA. This organization provided written consent for the use of all survey data pertaining to these dogs.

JS initiated the research, proposed the idea, and drafted the paper. DD performed the analysis, wrote up the results, and edited the paper.

The research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. The copyright for the C-BARQ instrument that was used as the source of behavioral information in the current study is owned jointly by the corresponding author (JS) and the University of Pennsylvania.