Comprehensive Psychoneuroendocrinology: Jennifer W. Applebaum, Evan L. Maclean, Shelby E. Mcdonald
Comprehensive Psychoneuroendocrinology: Jennifer W. Applebaum, Evan L. Maclean, Shelby E. Mcdonald
Comprehensive Psychoneuroendocrinology: Jennifer W. Applebaum, Evan L. Maclean, Shelby E. Mcdonald
Comprehensive Psychoneuroendocrinology
journal homepage: www.sciencedirect.com/journal/comprehensive-psychoneuroendocrinology
A R T I C L E I N F O A B S T R A C T
Keywords: Love and strong social bonds are known buffers in the experience of adversity. Humans often form strong bonds
Human-animal interaction with non-human animals. The human-animal bond refers to a mutually beneficial and dynamic relationship
Adversity between humans and non-human animals. Previous research suggests that strong bonds with pets may promote
Multispecies families
resilience in the experience of adversity, but a strong bond with a pet can also complicate this very experience of
Pets
Companion animals
adversity, particularly among low-resourced and disadvantaged populations. What is the role of the human-
Human-animal bond animal bond in adversity, and what is the role of adversity in the bond between a human and a non-human
animal? In this article we outline the state of research on the role of various types and sources of adversities
in multispecies households (i.e., families, relationships) to consider this overarching question. We focus specif
ically on intimate partner violence, housing discrimination, LGBTQ+ identity-based discrimination, racism,
neighborhood disadvantage, and economic inequality. We then outline an agenda for future research about love,
adversity, and multispecies relationships, and discuss implications for public policy and community-based
interventions.
1. Introduction serve as sibling figures for children [3–8]. In this vein, there is a growing
movement away from anthropocentric views of family systems and to
In contemporary society, love comes in many forms, including ward an increasing recognition of multispecies families and households
attachment bonds between people and their pets.1 Evidence of our close [9,10].
bonds and kinship with other species manifests in many ways. Particu
larly notable in the United States is the prevalence of cohabitation with
pets and growing recognition of the modern, multispecies household.2 1.1. Overview
Indeed, it is estimated that approximately 60% of people in the U.S. live
with a pet, a majority of which consider their pet(s) to be a member of Love and strong social bonds are known buffers in the experience of
the family [1,2]. Dogs and cats are the most prevalent animals kept as adversity [11–16]. However, the literature to date has failed to
pets in the U.S., residing in approximately 46% and 25% of homes, adequately consider how love that is characterized by the bond between
respectively [1]. Adults’ social and emotional relationships with pets are a human and non-human animal (i.e., pet) impacts the lived experience
often akin to a parental relationship with a child, whereas pets may of adversity. There is some evidence that strong bonds with pets may
buffer stress and promote resilience in adverse social contexts. However,
* Corresponding author.
E-mail address: [email protected] (J.W. Applebaum).
1
In the interest of brevity and consistency, we chose to use the term “pet” throughout this essay to refer to a non-human animal that lives alongside a human or
humans. This term is synonymous with the term “companion animal.”
2
In this essay we use the terms “multispecies household,” “multispecies family,” “multispecies bond,” and “multispecies relationship” interchangeably to refer to
the unit characterized by the relationship or bond between a human (or humans) and a non-human animal (or animals) who typically coexist together. We use these
terms to refer to the family or household unit, though “household” does not necessarily refer to those contained within a house (i.e., we include unhoused individuals
and their animal companions in these descriptions), and “family” does not necessarily refer to more than one individual and one animal, nor does it necessarily refer
to those who would be recognized legally as family.
https://doi.org/10.1016/j.cpnec.2021.100071
Received 1 April 2021; Received in revised form 1 July 2021; Accepted 5 July 2021
Available online 7 July 2021
2666-4976/© 2021 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
J.W. Applebaum et al. Comprehensive Psychoneuroendocrinology 7 (2021) 100071
strong bonds with pets can also complicate adverse situations, and human-animal bond (HAB), a term defined as the, “mutually beneficial
create barriers to meeting the social, emotional, and basic needs of both and dynamic relationship between people and other animals that is
the individual and their pet. Our overarching argument is centered influenced by behaviors that are essential to the health and wellbeing of
around the assertion that adversity interacts with the human-animal both” [18]. It is hypothesized that human-pet dynamics satisfy needs in
bond to create a complex interplay of disadvantage and resilience (see both humans and animals for companionship, emotional support,
Fig. 1 for a visual representation). In this article we focus specifically on nurturing and love [19–21]. However, the reciprocal nature of this dy
relationships between people and pets. We do not address issues con namic is most applicable to relationships with pets that share mamma
cerning service animals, emotional support animals, or other working lian social cognition and emotion. The neural and anatomical systems
animals, though we recognize that individuals often form strong that serve as mechanisms of positive sociality are shared among humans
emotional bonds with working animals. Importantly, in some cases the and their most preferred domestic species (e.g., dogs), and likely permit
issues we discuss below will also apply to working animals when the line the development of strong HABs [22,23]. In addition to this evolu
between working animal and pet may blur (e.g., when the handler of a tionary perspective, multiple theoretical orientations have been applied
service dog develops an emotional attachment with the dog, see [17]). to understand the love people have for their pets. Attachment and social
The purpose of this essay is threefold: (1) first, we review current support theory, in particular, are often applied as frameworks for
theoretical orientations toward explaining relationships between identifying underlying biobehavioral and social mechanisms through
humans and non-human animals. We follow with a working definition, which interactions with pets may be beneficial [24,25]. Broadly, the
and explanation of our orientation toward the construct of adversity. (2) application of these theories emphasize that humans and animals
Next, we review select literature concerning human-pet relationships develop social bonds (attachment) and that relationships with animals
and adversities in many forms. (3) We set an agenda for future research provide indirect (facilitation of human interaction) and direct (e.g.,
with the goal of further understanding the myriad ways in which adverse positive regard and companionship) forms of social support to humans
experiences and scenarios may impact people, pets, and their shared [25–29] (see Ref. [30] for a review). It is well documented that, across
bonds within multispecies relationships. We conclude with recommen the lifespan, interactions with pets provide their human companions
dations for public policy and community partnerships aimed at allevi with a sense of social support that mirrors that of attachment bonds with
ating some of the adversities faced by multispecies families. other people, yet offers unique characteristics that diverge from the
complex dynamics of human interactions.
2. Theoretical orientations toward explaining the human- One of the unique characteristics of human-animal relationships is
animal bond that pets are often perceived by humans as being a reliable, nonjudg
mental source of companionship and support, especially in the context
A driving factor of the prevalence of multispecies families is the of stressful situations or adversity [31–34]. As a result, children and
Fig. 1. Conceptual relationships between the human-animal bond, interpersonal adversities, resilience, and social inequalities as they impact multispecies re
lationships. Quotes to illustrate these relationships are excerpts from the authors’ qualitative research.
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J.W. Applebaum et al. Comprehensive Psychoneuroendocrinology 7 (2021) 100071
adults often seek out interactions with their pets in times of stress if the of minority stress are considered to have particularly harmful impacts on
animal provides a sense of comfort, consistency, or safety. It is hy short- and long-term adjustment (e.g., psychological and physical
pothesized that the benefits of human-animal interaction (HAI), a term health) [49–53].
often used to refer to any situation (e.g., interactions with household Adversity increases an individual’s risk for a variety of negative
pets, interactions with therapy animals) where there is contact between health and social outcomes, such as poor psychological and physical
humans and animals [18], may be most pronounced when individuals health outcomes and housing and economic insecurity [49–53].
are in a “stress state” [22], which makes human-animal relationships Broadly, it is argued that dysregulation of the stress response system is a
particularly important to consider when evaluating vulnerability and common mechanism underlying links between adversity (particularly
resilience to adverse experiences. early life adversity) and poor health outcomes. Specifically, this occurs
At a biological level, bonds between humans and pets are hypothe via impacts on the HPA axis and autonomic nervous system, including
sized to rely on neuroendocrine pathways involving oxytocin and developmental programming of the oxytocin and glucocorticoid systems
vasopressin, molecules that play critical roles in mammalian emotions [54,55]. These biological consequences include, but are not limited to,
and social behavior. In the brain, these neuropeptides act as neuro compromised neuroendocrine functioning (through alterations in pat
transmitters and neuromodulators, with important actions in limbic terns of release or epigenetic modifications to receptors), inflammation,
regions and the autonomic nervous system [35]. Both peptides are also and dysregulation of the immune system [56,57]. The ways in which an
released peripherally, where they act as hormones and provide feedback individual’s physiological system responds to changing environmental
to the central nervous system. Although previous research has focused demands, such as adverse experiences, produces changes that may be
largely on prosocial functions of oxytocin, both oxytocin and vaso adaptive short-term, but maladaptive at later periods of development or
pressin play important (and sometimes opposite) roles in stress and fear, in other contexts. Specifically, from a functional perspective, stress re
making them highly relevant for our understanding of biological re sponses mobilize energy reserves facilitating one’s ability to mount a
sponses to adversity in the context of HABs. defense to a threat. Though highly adaptive in the short term, chronic
Pendry and Vandagriff provide an important framework from which stress diverts energetic resources required for growth, digestion, and
to understand the biobehavioral mechanisms through which HAI at repair, leading to life history tradeoffs with deleterious consequences in
tenuates the stress response system [36]. Building on prior research, the long term [58,59].
they proposed the HAI-HPA (Hypothalamic–pituitary–adrenal axis) In addition, adversity may influence the characteristics of the HAB.
Transactional Model which posits that the socio-emotional support For example, selective social behavior and strong bonds with pets may
provided by pets buffers the stress response both prior to and after form in response to adversity and the perception that one’s welfare is
activation of the stress response system. They suggest that this ulti dependent on the presence of the other [22]. Positive social relation
mately disrupts the association between stress and concomitant psy ships and social support have particular value in the context of adver
chological maladjustment. Pendry and Vandagriff emphasize that the sity; the ability to manage stress is inextricably linked with social
presence of an animal may assist people in perceiving potential stressors behavior and engagement [22]. Indeed, it is hypothesized that HAI may
as less threatening [36]. This can, in some circumstances, prevent the potentially reverse some of the harmful impacts of chronic stress by
activation of the stress response system completely. Although Pendry contributing to functional increases in oxytocin or its receptor [22,60,
and Vandagriff focus on cortisol release as an end product of the HPA 61].
axis, it is important to note that HPA activity can be significantly Despite rapid growth in research and theory regarding the HAB, and
attenuated by oxytocin, or stimulated by vasopressin, through their benefits of HAI, few studies have considered how HABs contribute to
actions in the central nervous system [37–39]. Given their hypothesized negative emotions, such as fear and stress responses, and how this may
roles in HAIs, both oxytocin and vasopressin may be key mediators of impact the stress response system, particularly among populations
stress physiology in this context. Although current evidence for this disproportionately impacted by adversity. Many people live in social
hypothesis remains limited, several studies report increased oxytocin environments (e.g., family and neighborhood contexts) that increase
and/or decreased cortisol or vasopressin concentrations after affiliative their risk of exposure to maladaptive and atypical forms of HAI. In these
contact between people and pets [40–43]. The HAI-HPA framework also situations, individuals may experience fear as a result of being exposed
posits that once the stress response system is activated, pets may support to potentially traumatic experiences (e.g., violent households) or
humans in re-appraising whether their situation is still stressful. This adverse situations (e.g., poverty) that threaten an individual’s ability to
cognitive reappraisal, together with increased social contact with maintain a relationship with a beloved pet and/or threaten the welfare
nonhuman animals may further dampen physiological arousal through of an animal to which an individual is bonded. Given that HAI involves
social buffering [30,36,43–46]. complex, dynamic emotions and behaviors, it is critical that research
consider the interplay between positive and negative experiences asso
2.1. HABs in the context of adversity ciated with the HAB, and the ways that multispecies relationships
impact, and are affected by, adversity. From a biological perspective,
The evolutionary and theoretical perspectives outlined above offer adversity is known to have long-lasting effects on many of the same
insights into the importance of humans’ social bonds with non-human pathways implicated in the HAB [62,63]. However, biological responses
animals in the context of adversity. In this article, we use the term under conditions of adversity may be opposite to those associated with
adversity to refer to adverse life experiences (hardships, challenges, the protective effects of sociality. For example, responses to chronic
misfortunes) that have the potential to influence human development in adversity may include upregulation of vasopressin or its receptors,
a way that disrupts typical development, compromises an individual’s facilitating defensive behavior, or together with oxytocin, selective so
adjustment, and/or has the potential to lead to undesirable outcomes cial bonds [63]. Thus, both the basal patterns of these neuroendocrine
[47,48]. Adversity can involve single forms of acute or chronic stress. systems, as well as their acute responses to HAI, may differ markedly in
However, given that adversity is typically experienced as multiple people experiencing chronic adversity.
events, rather than a single experience, it most often involves a combi
nation of acute and chronic stressors, some of which are preventable or 3. What we currently know about the interplay of adversity and
malleable and others that are not. Among forms of adversity commonly multispecies relationships
studied, poverty, household dysfunction (e.g., exposure to domestic
violence, substance use), psychological, physical, and sexual forms of In this section we review literature on the interactions between
abuse, neighborhood dysfunction (e.g., neighborhood violence, crime), adversity and multispecies bonds, and the resulting impact on people
and experiences of racial and/or ethnic discrimination and other forms and pets within these relationships. We pay specific attention to the
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J.W. Applebaum et al. Comprehensive Psychoneuroendocrinology 7 (2021) 100071
ways that love and fear interact within these multispecies households (i. choose to maintain their relationship or living situation with their
e., families, relationships) to result in greatly varied health and well abuser out of fear for their pet and what might happen to the animal in
being outcomes for all household members, including both human and their absence [31]. This compromises the safety of all victimized
non-human animals. We recognize there are myriad sources and con members of the family, including beloved pets.
tributors to adversity, as well as responses to them. These adversities
range from interpersonal trauma to systemic inequalities, which can 3.2. Housing discrimination
interact and accumulate to result in extremely varied and individualized
experiences. Additionally, we recognize that individuals and groups are Access to affordable housing in the U.S. is a widespread problem. It is
often represented by various social categorizations, which can combine estimated that, as of 2020, over 50% of renters in the U.S. were
for varied experiences of disadvantage or privilege (see: intersection considered “rent burdened,” which is defined as spending more than
ality [64]). Although we do not specifically consider intersectionality in 30% of monthly income on rent [81]. Housing insecurity has only
this paper, it is implied at times throughout. In the interest of limiting worsened during the COVID-19 pandemic, as an estimated 30–40
our scope, we have chosen to focus the below literature review on the million renters are facing eviction in 2021 [82]. While some munici
following topics: intimate partner violence, housing discrimination, palities have placed restrictions on the amount of extra monthly rent a
LGBTQ+ identity-based discrimination, racism, neighborhood disad landlord can officially charge for allowing a pet on the property, these
vantage, and economic inequality. ordinances are uncommon. Moreover, pet ownership does not qualify as
a protected status or identity under the Fair Housing Act, therefore,
3.1. Intimate partner violence there are no sweeping regulations nor policies that protect multispecies
families from discrimination on the basis of including a non-human
Few areas of research demonstrate the intersection of love, fear, and animal. Policies restricting the number, type, and size of family pets in
the HAB as effectively as studies on the link between intimate partner rental units and condominium associations are extremely common. In
violence (IPV) and animal cruelty. IPV is a form of family violence 2005 Carlisle-Frank, Frank, and Nielsen estimated that only 9% of the
characterized by a variety of behaviors within an intimate relationship rental housing stock in the U.S. was “pet-friendly” in that it had no re
that are intended to assert control and power over another individual. strictions on any pet-related factors, while 44% had limited pet allow
These behaviors include psychological, physical, and/or sexual harm by ance, and 47% allowed no pets at all. The study, along with a similar
a current or former intimate partner [65–67]. IPV occurs among all study in 2018, found that pet-friendly rental units had higher average
forms of contemporary intimate relationships. However, in this section rent and higher average deposits than properties that did not allow pets,
we highlight studies of the statistically more prevalent, and more and pet-owning renters often settled for lower-quality housing in less
frequently reported, scenario of a woman being victimized by a male desirable locations [83,84].
partner. Nearly 24% of women in the United States will experience IPV The above issues are reflected in recent studies: pet ownership is a
during their lifetime [68] during which they may experience numerous common barrier to finding and maintaining affordable rental housing
tactics of coercive domination and retaliation, including a partner’s both within the U.S. and elsewhere. The experience of renting with pets
intentional harm or threat to harm animals as a form of psychological can itself cause perceived feelings of insecurity and instability, some
abuse of them, their pet, and/or their children [31,65,66,69–74]. times even prompting renters to hide pets from landlords, thereby
Across studies, it is estimated that 25%–71% of IPV survivors with putting themselves at an increased risk of eviction if the pet is discovered
pets report having experienced violence toward an animal by their [85]. The effects of lower-quality, limited availability, and higher price
abusive partner [75,76]. Faver and Cavazos surveyed women receiving tags for rental pet-friendly rental housing, compared to properties that
domestic violence shelter services and found that among women who restrict pets, also contribute to internalized feelings of instability among
did not report maltreatment of pets by their partner, 51% indicated their renters [86]. Pet owners with more resources have the option to be se
pet was an important source of support. In contrast, 88% of participants lective in rental properties, while those with less resources are often
who reported animal maltreatment by their partner identified the mal forced to accept lower-quality housing or avoid contacting the property
treated pet as a “very important” source of emotional support [77]. manager for repairs for fear of being considered a nuisance (regardless of
Results of this study and others suggest that a victim’s love for their pet the involvement of the pet in the issue) [86].
(s) may be a prominent factor in violent perpetrators’ motivation to The problem of renting with pets is especially salient for families and
engage in animal cruelty [31]. Adding to the psychological burden of individuals who are already facing other forms of disadvantage, such as
experiencing IPV and concomitant animal cruelty, adult victims often discrimination and/or resource constraint. Rental units that restrict pets,
witness their child(ren)’s abuse of pets in the home. Children who are or certain types of pets, are more common in disadvantaged commu
exposed to animal cruelty are more likely to engage in aggressive and nities and communities of color [87]. Additionally, pet policies are not
cruel behaviors towards pets, making the emotional experience of being regulated within supported housing for older adults, such as assisted
subject to IPV behaviors and concomitant animal cruelty even more living facilities or nursing homes, and those who wish to age-in-place (i.
psychologically burdensome and traumatic for adult victims who also e., in communities versus supported housing) with their pets may also
care for children. find it difficult to find appropriate housing. Toohey and Rock [88]
Numerous qualitative studies suggest that adult and child survivors illustrate the need for what they call “more-than-human solidarity” in
of IPV live within a duality of finding support in their bond with a pet housing policy in order to support economically vulnerable older adults
while also experiencing chronic fear and guilt about having that bond in multispecies families. They found that older adults would often risk
exploited by their partner [31,78]. Victims of IPV are often socially their own health and wellbeing in order to preserve the relationship with
isolated from friends and family, and for both youth and adults an ani their pet(s). In some cases, pet owners who cannot find affordable
mal companion may be their only form of consistent and reliable housing that can accommodate their pet(s) are forced to choose home
emotional support and stress-reduction [33,79]. The close bonds that lessness in order to avoid having to relinquish, re-home, or abandon
arise between people and their pets in psychologically and physically their pet(s) [89]. Housing issues are a frequently-cited reason for shelter
abusive living situations may lead adult and child survivors to become relinquishment of pets [90]. Further, those who do find themselves
engaged (physically, verbally, as a means to protect their pet) in in unable to access housing due to pet ownership (and/or other issues) may
cidents of animal cruelty, which may increase their risk of physical also find their pets prevent them from entering sheltered housing or
injury and/or death by an abusive partner [31–33,80]. Moreover, in the accessing health and social services [91]. This can pose a particularly
absence of access to pet-sheltering or pet-fostering services, pet-friendly difficult situation as pets are known to be important supports and mo
alternative housing, and/or financial resources, victims of IPV may tivators for those in very precarious situations, such as people who are
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J.W. Applebaum et al. Comprehensive Psychoneuroendocrinology 7 (2021) 100071
unhoused [92,93]. Pets are often cited as a source of resilience and peers, and new acquaintances [34].
motivation for maintaining health for those facing substantial hardships, Despite these benefits of HAI, the subtle and overt forms of minority
such as homelessness [93], a diagnosis of HIV [94], and identity-based stress that are disproportionately prevalent in the daily lives of LGBTQ+
discrimination, upon which we elaborate below. people may make this population more vulnerable to potential hardships
associated with pet ownership. The aforementioned qualitative study of
3.3. LGBTQ+ identity-based discrimination 117 LGBTQ+ young adults also found that 90% of the sample reported
stress associated with living with or caring for pets (behavioral prob
The dynamic interplay of love, fear, and HABs is also demonstrated lems, impact on expenses, impact on social relationships) and that these
in literature on HAI in marginalized populations, such as historically stressors were salient and influential experiences that compromised, or
(and currently) underrepresented groups (e.g., racialized minority had the potential to compromise, wellbeing via emotional and financial
populations, sexual and gender minority populations, etc.). However, burdens [34]. In that study, more than 60% of the sample recounted
few studies have examined how the experiences of risk and resilience caregiver burden associated with meeting pets’ needs, such as medical
associated with living with pets may be impacted by the unique stressors and behavioral health issues, being able to secure an alternative care
and sociocultural context faced by individuals who hold marginalized giver in emergency situations, and having difficulty managing finances
identities [34]. In this section, we review the emerging literature on HAI as a result. More than half also described psychological stress associated
among sexual and gender minority groups (e.g., lesbian, gay, bisexual, with loss, potential loss, and/or harm to their pet; some even disclosed
transgender, queer, and other marginalized sexual and gender identities, ruminating of when their pet would die, and feared if they would be able
or “LGBTQ+“) to demonstrate additional ways in which love for pets and to cope and adjust to that life transition. This form of stress is particu
multispecies relationships are shaped by adversity. We also highlight larly concerning among populations, such LGBTQ+ communities, that
ways in which HAI may operate as a risk and protective factor in the experience increased risk for psychological stress and maladjustment,
context of sexual and gender minority stress. barriers to affirming healthcare, and an increased likelihood of experi
Emerging evidence suggests that the risks and benefits of living with encing poverty and reduced social support [121,122].
pets may be particularly salient for LGBTQ+ individuals. LGBTQ+ Although pets may be an important source of social support and
communities experience disproportionate risk for adversity (e.g., companionship that can promote resilience in the context of adversity,
employment discrimination, housing insecurity, family and peer rejec multispecies families experience unique challenges that have the po
tion) and a broad range of health disparities which stem from oppressive tential to exacerbate vulnerabilities that result from systemic in
sociocultural structures and attitudes toward LGBTQ+ people; the equalities. The degree to which bonds with pets may exacerbate
experience of navigating cis-heteronormative social contexts and asso vulnerability, particularly in the absence of essential resources is dis
ciated stressors is often called minority stress [34,95–97]. Minority cussed further below. Next, we discuss the degree to which comfort and
stress broadly includes varied adverse experiences that occur in overt coping through HAI may be compromised by another form of adver
and covert forms, such as discrimination, victimization, social rejection, sity—racism.
and internalized stigma [98,99]. The accumulation of minority stress
contributes to LGBTQ+ youth and adults’ increased risk for a broad
3.4. Racism
range of physical (e.g., obesity [100]), behavioral (e.g., substance use,
risky behaviors [101]), and mental health (e.g., internalizing behavior
We begin this section with a statement regarding our own position
symptoms, suicidal ideation [102,103]) disparities. Such outcomes are
ality: the authors of this essay identify as White, therefore, we
inextricably linked with other outcomes of oppression, such high rates of
acknowledge that we cannot fully appreciate nor understand the expe
housing instability and economic insecurity in this population
rience of pet ownership for people of color.3 That said, we feel it is
[104–107].
necessary to draw attention to these ongoing issues of social injustice as
Social support (quality and number of confidants) and belongingness
they are inherently related to love, fear, and the HAB. Issues of housing
are important factors that promote healthy identity development and
and economic inequalities, which we cover in other sections, are also
resilience in this population [108–112] as well as known buffers of the
deeply and inextricably linked to historical and ongoing marginalization
association between adversity and mental health problems [113–115].
on the basis of race and ethnicity. Here we discuss other salient examples
Studies indicate that pets are frequently considered to be “chosen fam
of chronic and acute adversities borne out of racism as they relate to the
ily” and confidants among LGBTQ+ individuals [116]. Furthermore,
HAB: the history of dogs as a tool of oppression, current discriminatory
several studies link pet ownership and other aspects of HAI with resil
practices in animal welfare, and social control via animal-related trauma
ience and positive coping in this population. Both pet ownership and
and violence. We focus our attention primarily on anti-Black racism,
positive engagement with pets have been identified as factors that
though we acknowledge that racism against other racial and ethnic
mitigate associations between familial victimization and psychological
groups is also a driver of inequities in the experience of multispecies
stress in studies of LGBTQ+ populations [117,118]. Moreover, a recent
relationships.
study of LGBTQ+ emerging adults found an indirect effect of exposure to
Race is a known predictor of pet ownership in the U.S.: according to
LGBTQ+ microaggressions on personal hardiness (an indicator of
recent population estimates, approximately 29% of Black individuals in
interpersonal resilience) via HAI [119]. Specifically, microaggressions
the U.S. own pets, compared to over 70% of White individuals [1]. Some
were associated with increases in HAI (as measured by comfort from and
may point to cultural differences to explain this disparity. Although we
attachment to pets); in turn, increases in HAI were associated with
agree that culture certainly plays a role in patterns of pet-keeping (see
higher levels of personal hardiness among these youth [119]. Another
[123]), here we discuss other possible explanations for this disparity
study of LGBTQ+ emerging adults found that the effect of identity-based
including deep roots in historical and systemic anti-Black racism, spe
victimization on self-esteem was moderated by the degree to which
cifically within the U.S. In discussing pet ownership among Black
participants sought out comfort from pets, such that victimization was
not related to decreases in self-esteem when participants reported
moderate to high levels of comfort from pets [120]. Such findings have 3
We use the term “people of color” per the American Psychological Associ
been mirrored in recent qualitative work that found nearly 74% of 117 ation guidelines (see: https://apastyle.apa.org/style-grammar-guidelines/bias
LGBTQ+ young adults who lived with pets reported that their pet was an -free-language/racial-ethnic-minorities) to refer to groups or populations who
important form of support that helped them positively cope with mi do not identify as White. We acknowledge there are inherent issues and dis
nority stress. In addition, youth reported that pets helped to promote agreements with terminology, and our hope is our language choice is such that
social capital and facilitate healthy interactions with family members, it will cause the least harm to marginalized individuals.
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J.W. Applebaum et al. Comprehensive Psychoneuroendocrinology 7 (2021) 100071
families and communities in the U.S., one must first acknowledge the mutually-beneficial and at times intuitive relationships with their pets,
ways in which dogs have been used as an historical tool of racial attending to one another’s needs and offering companionship [130].
oppression (see Refs. [124–126] for in-depth discussions of these topics).
Dogs were used by slave owners to intimidate, control, and even kill 3.5. Neighborhood disadvantage
Black people in the American south during the era of slavery. The legacy
continued into the civil rights era when dogs were routinely used by A widely-cited study by Wood and colleagues outlines a potential
police to violently quell public demonstrations protesting racial segre mechanism for the ways in which pets may be beneficial to health: social
gation [126]. In fact, these patterns persist in contemporary society. For capital [140]. Social capital is considered to be the extent to which an
example, in a 2015 report by the U.S. Department of Justice following individual is connected and embedded within their communities and
the police killing of Michael Brown found the Ferguson, Missouri police social networks, and is a robust predictor of physical and mental health
department had a notable “… pattern of deploying canines to bite in outcomes [141]. Wood and colleagues found that, among their Austra
dividuals when the articulated facts do not justify this significant use of lian sample, pet owners tended to report stronger and more frequent
force” (p. 31), and that every victim of the police dog incidents were social connections within their neighborhood and community, which
Black [127]. There were also reports of police dog intimidation during was considered to be connected to interactions involving pets. These
the Black Lives Matter protests in Ferguson as well as the uprisings in findings were replicated a decade later in the U.S., leading the authors to
2020. In using the term “culture” to explain low rates of pet ownership once again conclude that pet ownership appeared to be a “conduit” to
among Black individuals in the U.S., one is inherently (though perhaps social capital, thereby benefiting the health and wellbeing of people in
unknowingly) invoking this violent, racist history. This history is also multispecies relationships [142]. Notably, while Wood and colleagues
inherently linked to the current demographic patterns of pet ownership, appear to have collected considerable demographic information from
as well as ongoing barriers to pet ownership for people of color. their respondents, they did not explore the potential moderating role of
The continued oppression and discrimination against people of color race on these associations. This may lead one to wonder, considering
is evident in current practices and assumptions within animal welfare, enduring racial housing segregation and the legacy of redlining: does the
subsequently limiting access to pet ownership for these populations social capital effect of pet ownership extend beyond White individuals?
[128]. While pet ownership may be less common among Black in Mayorga-Gallo argues that, while White residents in Durham, North
dividuals, compared to White individuals, to our knowledge there is no Carolina, USA did experience social capital benefits of pet ownership,
evidence for racial or ethnic differences in the ways that pets are related the non-White residents of the same community did not, and in fact
to and cared for, barring issues of economic resources and agency (e.g., routinely experienced negative pet-related interactions with their White
access to veterinary care), among U.S. populations [129–131]. However, neighbors [143]. The very social connectedness experienced by White
for many animal welfare and control organizations, race does factor into pet owners was used as a tool to draw racial and ethnic boundaries and
perceptions of who should own pets, or who is considered a “responsible maintain racial distance in their multiracial community [143].
pet owner” [128,132]. For example, Guenther [133] argues that pit bull Spatial context, dubbed “neighborhood effects” in social science,
type dogs are broadly conceptualized as companions to Black and Latinx refers to the geographic contextual and ecological factors that influence
men, which has been used by some to rationalize discrimination against the social lives of the individuals located within the geospatial bounds
owners of pit bulls (i.e., Breed Specific Legislation, “dangerous dog” [144]. This concept has been extended to human-animal relationships to
clauses), as well as high rates of pit bull shelter euthanasia. Pit bulls in show that contextual factors determined by spatial analysis influence
particular have been subject to ongoing misconceptions regarding their the chances of a pet being separated from its family and ultimately
proclivities and traits. Some have argued this can be traced to their admitted to the shelter. For example, Ly et al. showed that contextual,
cultural association with men of color, and how racial bias and spatial factors such as quality of housing, economic disadvantage, and
oppression may manifest via some animal welfare practices (see unemployment (among other factors) predicted patterns of shelter
[134–136]). relinquishment from various neighborhoods in the Vancouver area
Beyond breed-specific discrimination, communities of color experi [145]. This was also reflected by Spencer and colleagues, who found that
ence disproportionate social control and punishment via institutional spatial patterns of child maltreatment were related to spatial patterns of
ized practices of animal control agencies, in addition to policing [132]. animal intake to a municipal shelter in a community in Florida [146].
For example, Hawes and colleagues found that the enforcement of the Both studies point to geographic patterns of social inequities, concen
city of Denver’s breed specific legislation (which banned pit bull type trated in areas of disadvantage, as significant risk factors for disrupting
dogs from 1989 to 2020) was most likely to occur in geographic areas the HAB and disadvantaging people and pets in multispecies
with notable racial tension between multiracial communities and those households.
that were predominantly White [137]. Notably, the practice of dispro
portionate enforcement of animal control policies and breed bans can 3.6. Economic inequality
lead to the confiscation or forced relinquishment of pets from the very
owners who may depend on them for emotional support due to their Economic inequality shapes the health and wellbeing of all members
experiences of chronic adversity [128]. Relatedly, in another example of of multispecies households. Among marginalized and disadvantaged
racialized trauma, Bloch and Martinez found that officer-involved people, the responsibility of pet ownership, and the experience of a bond
shootings in Los Angeles that resulted in the death of a dog (i.e., lethal with a pet, may compete with other priorities for limited resources. This
police shootings of dogs) were clustered in low-income communities of phenomenon creates an extra vulnerability in the face of adversities.
color [138]. Not only do communities of color experience dispropor Previous studies suggest that economically disadvantaged pet owners
tionate trauma via violence toward family pets, they are also subject to a will be more likely than other pet owners to risk their own health and
disproportionate share of state violence from police dog attacks [139]. safety in order to prioritize their pet(s), particularly when the individual
In the context of racism, pets (particularly dogs) can be both a source of has a strong bond to their pet (e.g. Refs. [91,93,147]).
trauma and adversity as administered by the oppressor, as well as a Stoltz and colleagues show that dogs have become actors within the
potential source of comfort and support for the oppressed. In an example “budgetary unit” of American families, therefore the family decision-
of the latter, a qualitative study with a sample of 15 women of color from makers are responsible for considering the dog’s wants and needs
various racial and ethnic backgrounds (i.e., nine Latinx women, two alongside that of human family members [148]. They assert that
Asian women, two Native American women, and two African American non-human animals kept as companions, and in particular dogs, have
women) found evidence for a common theme of “reciprocity” between shifted in American society to be conceptualized as actors who consume
pets and owners [130]. The women of color in this study described with people, whose wants and needs are included in the resource
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J.W. Applebaum et al. Comprehensive Psychoneuroendocrinology 7 (2021) 100071
budgeting of the household [148]. Pets, due to their liminal status of people. This assumption fails to recognize the unique effects of how
family/property, as well as animal control laws and policies, are identity and HAI play out in everyday life. Notably, we are unaware of
vulnerable and wholly dependent upon human caretakers throughout any research concerning the potential moderating role of comfort from
the entirety of their lives. If their guardian fails to care for them, they are pets on the relationship between experiences of racial or ethnic
usually subject to impoundment or abandonment, and often untimely discrimination and wellbeing among people of color. This topic warrants
death via euthanasia (in the case of sheltering) or neglect (if aban investigation. Second, there are myriad validated measures concerning
doned). This could lead economically vulnerable pet owners to make constructs like attachment to pets and comfort from pets (see [152])
choices that may appear irrational, such as allowing their own health however, the field needs better tools for measuring the negative aspects
and wellbeing to suffer, while prioritizing the health, welfare, perceived of HAI and the HAB. Notably, the “Perceived Costs” subscale from the
wants, and/or needs of their pets. These patterns are reflected in re Monash Dog Owner Relationship Scale (MDORS [153]) is useful for a
sponses to emergencies and disasters: bonded pet owners are at a higher generalized measurement of some of the potential drawbacks of dog
risk of failing to evacuate their homes if they are unable to bring their ownership, specifically. However, the MDORS lacks specificity with
pet(s) with them, as owners who have less resources at their disposal are respect to understanding myriad potential pet-related stressors and is
also less likely to have access to pet-friendly hotels or friends or family not generalizable to other types of pets. For example, a quantitative
who can temporarily offer their family shelter [149–151]. The public measure of pet-related stress reflecting themes in recent qualitative
health emergency posed by COVID-19 complicated healthcare planning studies, such as issues related to caring for pets with behavioral issues, or
for pet owners, as some reported they would not be able to seek emer difficulties balancing pet caregiving with other priorities and re
gency care out of concern that contingency accommodation for their sponsibilities (see [154–157]) would be useful for survey researchers
pets might not be available; this fear was especially salient for pet interested in a better understanding of the entire experience of pet
owners who had limited socioeconomic resources, and those who re ownership. Third, theoretical models that aim to identify the mecha
ported a strong attachment bond to their pet [147]. nisms through which HAI benefits human health and wellbeing pri
Guenther outlines the concept of “the irresponsible owner,” which marily focus on the benefits of touch and support in downregulating
Guenther dubs a myth, in The Lives and Deaths of Shelter Animals physiological reactions to stress. However, we argue that the general
[128]. Guenther posits that the construct of responsible pet ownership izability of these theories will remain limited if chronic and acute
permeates animal welfare and sheltering. This in turn places individual stressors related to the HAB are not accounted for in studies that test
responsibility upon pet owners for the (alleged) insufficient care of pets, these frameworks, particularly in the context of studying relationships
which often results in shelter relinquishment or field intakes by animal with household pets. Currently we know little about how adversity in
control officers when pets are found free-roaming in communities. teracts with the physiological systems that are hypothesized as central to
Guenther’s main argument centers around this misplaced blame and the HAB. However, preliminary studies of animal-assisted interventions
subsequent labeling of whole populations (characterized often by in populations that have suffered from trauma reveal effects that are
race/ethnicity and/or socioeconomic status) as “irresponsible” and sometimes opposite to those in other populations [158]. Given that
therefore unworthy of the companionship of a dog or cat. Guenther of many neuroendocrine pathways implicated in HAI can also be modified
fers an alternative explanation: the mechanisms of social control, by trauma or chronic stress [54,159], it is reasonable to expect that
oppression, and structural inequality place economically disadvantaged biological responses to HAI will vary significantly between populations.
(and usually Black and/or Latinx) pet owners in a state of precarity, Thus, studies with convenience samples may fail to adequately capture
thereby subjecting them to acute and chronic adversity (e.g., housing key psychological and physiological features of the HAB in the context of
instability, deportation, involvement in the justice system) that often adversity.
results in the forced separation of pet and (human) family, regardless of
how much they wish to preserve that relationship [128]. Notably, eco 4.2. Demographic patterns of pet ownership: uncovering mechanisms
nomic inequalities are rarely considered in HAI research to date. We related to adversity
discuss this in more detail, as well as other directions for future research,
in the following section. As we discussed above, population estimates of the demographic
correlates to pet ownership in the U.S. show that non-Latinx White in
4. An agenda for future research dividuals tend to own pets at much higher rates than do people of color,
particularly Black individuals [1]. Future research should further
Researchers interested in adversity and multispecies bonds face a interrogate why this disparity exists, particularly if pets may be
multidisciplinary field with somewhat disjointed methodological and health-promoting for those experiencing adversity and trauma. For
theoretical traditions. Here we detail three topics we feel warrant example, we currently have a very limited understanding of the (un)
additional research, and make recommendations for future directions. availability of pet-friendly rental housing (for analyses in North Carolina
We build upon the current state of research outlined in previous sections see [87]; Edmonton see [160]) and the racial and socioeconomic dis
to investigate the interplay between adversity and the HAB. tribution of these properties. However, a more comprehensive, nation
wide analysis is necessary for understanding the larger picture of the
4.1. The impact of pets on human wellbeing: better understanding the role barriers of pet ownership to low-income and historically marginalized
of adversity individuals. Additionally, more research related to HAI and racial and
ethnic discrimination is warranted, both regarding anti-Black racism, as
The field of HAI has been wrestling with an ongoing question for well as other minoritized groups. Researchers may consider integrating
some time: are pets good for human health and wellbeing? Currently, the concept of intersectionality in these endeavors (see [64]). Re
the thrust of the overarching question is in the realm of for whom, under searchers should also consider how the species of pet may factor into
what conditions, and also, why for some and not others? We posit that, in these relationships, as the hardships and barriers experienced for dog
order to get at these questions, researchers must better understand the owners may be fundamentally different from those experienced by
role of adversity in multispecies relationships. Here we recommend a reptile owners, for example. Similarly, different species might differ in
few avenues of potential exploration. First, we urge HAI researchers to their potential to be beneficial for social support or stress buffering in the
direct efforts toward better understanding HABs in marginalized pop experience of hardship and adversity.
ulations with the goal of exploring the interaction of stressors and sup Animal welfare organizations such as the Humane Society of the
ports associated with HAI. It is our belief that a false assumption has United States (HSUS) and the American Society for the Prevention of
been made in considering the effects of HAI to be comparable for all Cruelty to Animals (ASPCA) have made great strides in the provision of
7
J.W. Applebaum et al. Comprehensive Psychoneuroendocrinology 7 (2021) 100071
veterinary care to vulnerable communities with the goal of empowering adversities can simultaneously strengthen and challenge the HAB, and
pet owners to maintain the health and welfare of their pets, and also suggested that our knowledge of the physiological mechanisms involved
prevent pet relinquishment to shelters. However, questions remain in HABs will remain limited without future studies focusing on
about the lasting impact of these programs, which are often provided on marginalized populations and experiences of adversity. We continue
a temporary basis and, due to funding limitations, are not permanent here with a brief discussion of two limitations in this article and
fixtures in their communities. Veterinary care is often expensive; low- conclude with recommendations for public policy aimed at supporting
income, and even “middle class” pet owners often cannot afford to people and pets in multispecies relationships.
provide their pets with regular healthcare that is recommended by the
veterinary industry. Thinking beyond questions of access and afford 5.1. Limitations
ability, as veterinary medicine (and the pet product industry) is a
business, researchers may find themselves wondering if the concept of We acknowledge three major limitations in this article. First, the
idealized pet health maintenance and welfare (e.g., the utility of goods majority of evidence we discuss pertains specifically to “Western” so
and services beyond basic health and welfare) is serving pets and their cieties. Future research should consider the role of adversity on human-
owners. We might ask: does the conceptualization of optimal pet health animal relationships in other parts of the world that we failed to
and welfare unintentionally reproduce racial and socioeconomic in consider in this article, in particular: non-Western nations. Second,
equalities in access to pet ownership? If so, how might we better support while we consider animal welfare and shelter outcomes in this article, a
marginalized and disadvantaged individuals in ways that serve both pet majority of the content is anthropocentric, that is, prioritizing the per
and owner? spectives and experiences of humans above those of non-human ani
mals. Much of HAI research suffers from this limitation (see [162,163])
4.3. Data to investigate adversity and multispecies relationships and we assert future research should consider non-human animal ex
periences in addition to those of humans. Third, we do not discuss
The availability of data is integral to research efforts for under adversity and HAB as it relates to relationships between humans and
standing the role of adversity in human-pet relationships, and more service animals, emotional support animals, or other working animals.
broadly, interactions between pets and people in society. We argue for We acknowledge there are indeed hardships and adversities for in
the inclusion of extensive HAI measures in large, probability-based data dividuals with disabilities who have relationships with these types of
collection efforts that allow for generalization to entire populations. animals (e.g. Ref. [164]) and therefore we recommend future research
Because HAI research has long relied on less rigorous sampling meth further consider those experiences and perspectives.
odology (and quite often nonprobability sampling), entire populations,
particularly those who are non-White and/or low-SES, are not repre 5.2. Policy implications
sented in the current HAI knowledge base. Along these lines, although
rigor in HAI has improved in recent years, there is a crucial need for Opportunities exist for public policy aimed at alleviating adversities
further longitudinal HAI research, as well as better understanding of pet placed on multispecies relationships. First, we recommend the inclusion
relationships beyond the simple dichotomy of pet owner versus non-pet of pet ownership as a protected status against housing discrimination. As
owner. Short HAI measures have been included in a handful of large we detail above, many of the barriers faced by multispecies families that
population surveys, such as the General Social Survey in 2018, the in turn force the separation of pets from their people originate in the
Health and Retirement Study in 2012, and the Panel Study of Income inability to find affordable rental housing and temporary shelter services
Dynamics’s Child Development Supplement in 2014 and 2019. How that allow pets. We predict that sweeping pet-friendly housing policy
ever, these HAI measures were overly simplistic and failed to capture the will make enormous strides in preserving multispecies bonds, particu
complexity of HABs and HAIs. While they did allow for the investigation larly among marginalized communities and those who experience
of some outstanding HAI questions, they were not administered to full disproportionate adversity. Additionally, communities should
samples, often had a limited availability of correlates due to data encourage the partnering of human social welfare services with those of
structure and survey scope, and had not undergone rigorous psycho animal services in order to provide support to the holistic family unit in
metric evaluations in diverse populations [1]. times of hardship and adversity. For example, the provision of tempo
Beyond gathering nationally representative data on HAI, careful rary boarding or foster services for pets of individuals who are tempo
attention must be paid to study design concerning marginalized and rarily unavailable to care for them due to hospitalization or other issues
disadvantaged (i.e., “vulnerable”) populations. For example, HAI re would prevent both the permanent separation of pets from their fam
searchers may consider methodology such as participatory action ilies, as well as alleviate barriers to entering in-patient healthcare or
research, which both involves the research participants in the process, as accessing other services (see Refs. [165–169] for discussions on the
well as empowers the research subjects to put the findings into action in impact of these types of interventions). Models for these services exist in
both practice and policy [161]. Researchers may also consider part various communities and can be replicated,4 but not without community
nering with community organizations that provide services to disad support and financial resources. Moving toward a model of support for
vantaged populations in order to assess their clients’ pet-related needs. the holistic family unit, inclusive of pets, is necessary for the mitigation
Further, simply bringing research findings to the attention of community of adversities and the promotion of the HAB.
stakeholders could encourage organizations to take needed steps toward
supporting people and pets together. Funding
8
J.W. Applebaum et al. Comprehensive Psychoneuroendocrinology 7 (2021) 100071
5R01-HD-66503-4, and 1L60HD103238-01. The content is solely the Interact, American Psychological Association, 2016, pp. 89–105, https://doi.org/
10.1037/14856-006.
responsibility of the authors and does not necessarily represent the
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