relationships with conspecifics may differ from those formed with humans, and research in this area is in its infancy. Behavioral indicators of attachment toward the dam have been identified and, in some circumstances, the stress response can be reduced by the presence of a cohabitant dog (Mariti et al. 2014, 2017). Cimarelli et al. (2019) suggest that it is the individuals involved, not the species type, who impact the quality of the bond. They observed that while referencing/information seeking was more often found in dog‐human relationships, both dog‐dog and dog‐human relationships shared similarities in terms of affiliation and stress alleviation (i.e., members of either species could provide more or less affiliation or stress alleviation). Taken together, dogs can have complex, amicable, and longstanding relationships with members of their own and other species. The potential for intra‐ and interspecies integration starts at the beginning of life.
1.3 Dog Behavioral Development
While genetics provide the blueprint for life, experiences—particularly those early in life—can impact dog behavioral development. Increased early life plasticity allows a growing dog to be affected by and responsive to environmental inputs, which in turn has the ability to affect immediate and future behavior. Understanding early life developmental periods goes hand in hand with identifying environments and experiences that support normal development and those associated with the development of pathological behaviors (behavior problems) and behaviors expressed out of context or excessive in terms of frequency, duration, or intensity (Dietz et al. 2018; Hammerle et al. 2015).
“Critical” or “sensitive” periods are specific weeks or months where behavior patterns emerge and environment, stimuli, and social exposure support development (Scott and Fuller 1965). Additionally, events during the prenatal period—such as in utero exposure to maternal stress—as well as subsequent dam care styles can influence puppy behavioral and cognitive development and later coping (Santos et al. 2020). While developmental periods have a clear progression (dogs will not play bow before opening their eyes), transitions between stages are more gradual than initially thought (Bateson 1979). The following periods are therefore guidelines—without hard‐and‐fast beginning and end points. Rates of development (heterochrony) can also differ among breeds. As well as among individuals.
1.3.1 Neonatal and Transitional Periods
In less than a month, pups move from complete dependence on the mother (zero to two weeks) to increasing autonomy (two to three weeks). Dogs enter the world without vision, hearing, or coordination, and they rely on tactile and simple olfactory sensations. They are unable to self‐regulate temperature and spend most of their time sleeping, nursing, and in physical proximity to the dam and littermates. Newborns display “kneading” or “swimming” behavior directed at the teat or milk source to attain food, and the dam initiates elimination by tactile stimulation. If isolated they make high‐pitched calls—whines or yelps—that indicate distress and are frequently described as care soliciting (Elliot and Scott 1961). These early vocalizations transform into high‐pitched, high‐frequency “alone barks” that are contextually similar and also elicit attention (Yin and McCowan 2004). At around two to three weeks, eyes and ears open, and characteristic “dog” qualities begin to emerge such as walking and tail wagging, rudimentary elements of play, and a startle response (Case 2005). An interest in solid food may begin, and anogenital licking is no longer required for elimination.
Dam maternal care styles throughout these early periods vary in quantity and quality and contribute to pup development (Dietz et al. 2018). Experiencing brief mild stressors beginning from birth—such as human handling and brief separations from conspecifics—could have long‐term beneficial effects on stress resilience (Gazzano et al. 2008). Brief, gentle exposure to social (human and non‐human animals) and asocial (auditory and visual) stimuli can further support physical and cognitive development.
1.3.2 Sensitive or Socialization Period
Week 3 to approximately week 12 is a time of immense growth, particularly for species‐specific social behaviors and learning opportunities. Approach and avoidance emerge early in this period, followed by more coordinated motor patterns, such as play fighting with littermates. Pups increasingly send and receive intraspecific signals, and vocalizations become more complex and are incorporated into social situations. Dogs identify littermate and species members, and social learning from conspecifics and humans has been demonstrated in puppies as young as eight weeks of age (Fugazza et al. 2018; Serpell et al. 2017). Pups also show attention to and interest in humans, and from an early age they can follow human communicative signals like gaze or pointing (Riedel et al. 2008). A period of interest and investigation can be followed by wariness or fearfulness, particularly after week 5 and culminating between weeks 8 and 10 (Case 2005). The presentation of fear could be modulated by factors such as genetics, individual coping styles, or early life experiences (Rooney et al. 2016).
Premature weaning and early separation from littermates are inadvisable. Separated dogs miss valuable social exchanges, both observational learning opportunities and feedback on their own behavior. Dogs vary in weaning time even within breed, and weaning prior to two months has been associated with subsequent behavior challenges such as increased destructive behavior and possessiveness, excessive barking, and fearfulness (Pierantoni et al. 2011).
As suggested, the socialization period is the time when dogs acquire “behavior patterns appropriate to the social environment in which [an individual will] live, allowing them to coexist/interact with other individuals” (Blackwell 2010). Dog interest and comfort with all that the human environment has to offer should not be assumed simply because dogs are “domestic.” Instead, socialization involves short, repeated doses of enjoyable, varied experiences and exposing pups to social and non‐social stimuli that will be part of their environment. Individual dog behavior should be closely monitored for indications of discomfort with consideration for under‐ as well as overstimulation (Howell et al. 2015). Pluijmakers et al. (2010) found that puppies between three and five weeks of age exposed to audiovisual playback—consisting of animate and inanimate objects and noises at normal volume—showed decreased fear of novel objects and unfamiliar settings compared to a control group who displayed increased stress‐related behaviors. Veterinary professionals recommend considering puppy socialization classes as early as seven to eight weeks and with a minimum of one set of vaccines (American Veterinary Society of Animal Behavior 2008). Early life restrictions can have profound effects on dogs. Numerous studies find that dogs raised in commercial breeding establishments (commonly known as “puppy mills” or “puppy farms”) or purchased from pet stores displayed ongoing behavioral and emotional challenges such as increased fear and aggression and difficulty with separation when compared to dogs not raised in such environments (McMillan 2017).
1.3.3 Juvenile and Adolescent Periods
The periods from approximately three to six months and six months to one to two years (during which sexual maturity occurs) have received much less attention than other developmental periods. The juvenile period is sometimes described as the secondary socialization period because, like early in life, experiences can affect developing personality. Harvey et al. (2016) conducted behavior tests with dogs at five and eight months and found that some traits like jumping, barking, and low posture during greeting were stable, while others such as obedience, lip licking, and body shaking were not consistent between the two periods. A retrospective examination of guide dog development found that owner‐directed aggression decreased in German shepherds, Labrador retrievers, golden retrievers, and golden × Labrador crosses from 6 to 12 months, but German shepherds showed an increase in stranger‐directed aggression during this period (Serpell and Duffy 2016). Reductions in trainability and responsiveness to owner commands have also been documented during these periods (Asher et al. 2020). Although they have long since shed their puppy appearances, these dogs are still very much in a period of transition and growth. The dog‐human relationship could benefit if people set
