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Introduction to Dog Behavior

Julie Hecht and Alexandra Horowitz

1.1 Evolutionary History of the Species

The domestic dog, Canis familiaris, is a member of the Canidae family, genus Canis, which also includes wolves, coyotes, and jackals. Canis lupus, the present-day gray wolf, is the domestic dog's closest living ancestor (Vilà et al. 1997), and the divergence began more than 10,000 years ago, possibly with early hunter-gatherers and then in association with early agriculture (vonHoldt and Driscoll 2017). The dog is the only domesticated species of the genus: that is to say, the only canid for whom artificial selection (selective breeding) by humans has usurped natural selection as a major mover of the species.

Considering dog behavior in the context of their wild cousins can at times clarify some common dog behavior. Wolves living among family members approach and greet those returning from hunting by licking-"kissing"-their faces. Licks are prompts for the wolf to regurgitate some of the kill just ingested. Similarly, a dog's "kiss" is a greeting, but it is also a vestigial interest in whatever it was an owner might have consumed since leaving the house (Horowitz 2009b). A dog's propensity to sniff peoples' genital area could be viewed as intrusive or "impolite," yet it is analogous to canids' olfactory investigations of the genital and anal areas of conspecifics, which contain information about the identification, and perhaps recent activities and health, of that individual (Sommerville and Broom 1998). At the same time, there are numerous differences between dogs and wolves, particularly regarding ecological niche and social organization (Marshall-Pescini et al. 2017), and analogies between the two should be made with caution. Instead, dogs' intimate association with humans has had a seminal impact on every aspect of their being.

1.2 Dogs and Humans

Canis familiaris and Homo sapiens share a special relationship. They engage in the seemingly mundane-walking side by side in a park-to the complex-running an agility course or alerting a hearing-impaired person to a ringing telephone. In recent years, cognitive, behavioral, and physiological studies have added clarity to this unique interspecific bond.

1.2.1 Dog Interspecific Social Cognition

Dogs display behaviors that can give people the feeling of a shared experience and mutual understanding. Dogs monitor human behavior closely, are sensitive to human actions and attentional states, and act in accordance with humans in coordinated and synchronized ways. For example, when unable to access a desired item, dogs may alternate their gaze between the item and a person to direct the person to retrieve it (Miklósi et al. 2000). Even as puppies, dogs readily respond to human communicative gestures, whether stemming from hands, the face, (e.g., the eyes), or other body parts (Reid 2009; Riedel et al. 2008). This propensity is even observed in some free-ranging dogs (Bhattacharjee et al. 2020), and personality, enculturation, and reinforcement history could also affect outcomes. Dogs take note of human attentional states from the eyes as well as head and body orientation-a dog being more likely to remove a muffin from a countertop if a person's back is turned or eyes are closed than if the person's eyes are open (Schwab and Huber 2006). Dogs discriminate human emotional expressions such as happy and angry faces (Müller et al. 2015). A number of dogs have proved extraordinarily attentive and responsive to human language (Kaminski et al. 2004; Pilley and Reid 2011). Not all dogs attend to verbal cues (Ramos and Mills 2019), and the emotional content, tone, and intonation of human vocalizations are particularly relevant. Behavioral synchronization-staying close to and moving in pace with a person-has been observed in owned dogs and, to a lesser extent, between shelter dogs and caretakers (Duranton and Gaunet 2018). Dogs and humans also play together, and these vastly different species can attend to each other's play signals; a dog's play bow-or a person's play lunge-is often responded to meaningfully (Rooney et al. 2001). People visiting a shelter searching for their new best friend may not be aware of the complex social exchanges underlying the dog-human relationship, but they may have experienced it with another dog and may even be seeking it out.

1.2.2 Dog-Human Relationships

Attachment theory initially described the affectionate bond relating to safety, security, and protection between a child and caregiver, and it has since been extended to and identified between dogs and their caretakers (Bowlby 1958; Topál et al. 1998). Attachment is displayed through particular behaviors such as proximity maintenance, approach, and gaze toward a caregiver when reunited. Similar to infants, dogs display the "secure base effect" by exploring and playing more in a novel environment when in the presence of an owner than a stranger (Horn et al. 2013). Like the child-parent relationship, dogs can display different attachment styles described broadly as secure (explore and also seek contact) or insecure (avoidant, ambivalent, or disorganized) (Solomon et al. 2019). Dog attachment style and owner caregiving strategies both contribute to the dyad's relationship (Rehn and Keeling 2016).

Early exposure to humans is important for normal dog social development, but attachment relationships can form later in life, multiple times, and toward multiple people. Gácsi et al. (2001) found that similar to owned dogs, shelter dogs displayed attachment behaviors toward a newly appointed "owner" (designated by three short interactions with the dog). Thielke and Udell (2020) found that, similar to owned dogs, dogs in foster care formed secure attachments, and leaving the shelter seems to further support relationship development. If adopters are concerned about shelter dogs forming bonds, these studies could provide comfort.

Biological mechanisms could also underpin the dog-human relationship. The neurohormone oxytocin is often highlighted for its role in bonding and affiliation, good feelings, and stress buffering. Studies find that pleasurable interactions such as gentle petting, light play, talking in a positive tone, greeting, and sharing gaze with a known person promote oxytocin release in both dogs and people (Kis et al. 2017; Powell et al. 2019b). Although oxytocin appears to contribute to the dog-human relationship, a positive oxytocin effect is not always observed (Powell et al. 2019a).

Researchers are also exploring whether administering oxytocin to dogs elicits affiliative and social behaviors. Findings to date are not straightforward. For example, Romero et al. (2014) found that oxytocin promoted affiliative behavior toward humans and other dogs, but Barrera et al. (2018) found that intranasal oxytocin did not improve reactions toward a stranger during a sociability test, as was expected. Additionally, administering oxytocin to dogs can be challenging, and Schaebs et al. (2020) found that a vaporizer mask-which requires training-administers oxytocin more reliably than the more commonly used intranasal spray. Regardless, unclear sex, neuter status, and breed differences have been identified, and outcomes are not always in the anticipated direction. In humans, for example, oxytocin has been linked to distrust of and preemptive aggression toward strangers (Sapolsky 2018). The utility and real-world use of oxytocin administration remains to be seen.

1.2.3 Relationships between Dogs

Dog 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...