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Biobehavioral responses to stress in females: Tend-and-befriend, not fight-or-flight

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Psychological Review Copyright 2000 by the American Psychological Association, Inc.
2000, Vol. 107, No. 3, 411-429 www.apa.org/journals/rev.html
Biobehavioral Responses to Stress in Females:
Tend-and-Befriend, not Fight-or-Flight
Shelley E. Taylor, Laura Cousino Klein, Brian P. Lewis, Tara L. Gruenewald,
Regan A. R. Gurung, and John A. Updegraff
University of California, Los Angeles
The human stress response has been characterized, both physiologically and behaviorally, as “fight-or-
flight.” Although fight-or-flight may characterize the primary physiological responses to stress for both
males and females, we propose that, behaviorally, females’ responses to stress are more marked by a pattern
of “tend and befriend.” Tending involves nurturant activities designed to protect the self and offspring that
promote safety and reduce distress; befriending is the creation and maintenance of social networks that may
aid in this process. The biobehavioral mechanism that underlies the tend and befriend pattern appears to
draw heavily on the attachment/caregiving system, and considerable neuroendocrine evidence from animal
and human studies suggests that oxytocin, in conjunction with female reproductive hormones and
endogenous opioid peptide mechanisms, may be at its core. This previously unexplored stress regulatory
system has manifold implications for the study of stress.
Survival depends upon the ability to mount a successful
response to threat. The human stress response has been
characterized as fight-or-flight (Cannon, 1932), and has been
represented as an essential mechanism in the survival process. We
propose that human female responses to stress (as well as those of
some animal species) are not well characterized by fight-or-flight,
as research has implicitly assumed, but rather are more typically
characterized by a pattern we term “tend and befriend.”
Specifically, we will suggest that, by virtue of differential parental
investment, female stress responses have selectively evolved to
maximize the survival of self and offspring. We suggest that
females respond to stress by nurturing offspring, behaviors that
protect them from harm and reduce neuroendocrine responses that
may compromise offspring health (the tending pattern); and by
befriending, namely affiliating with social groups to reduce risk.
We hypothesize and consider evidence from humans and other
species to suggest that females create, maintain, and utilize these
social groups, especially relations with other females, to manage
stressful conditions. We suggest that female responses to stress
may build on attachment/caregiving processes that downregulate
sympathetic and hypothalamic-pituitary-adrenocortical (HPA)
responses to stress. In support of this biobehavioral theory, we
consider a large animal and human literature on neuroendocrine
responses to stress, suggesting that the tend and befriend pattern
may be oxytocin-mediated and moderated by sex hormones and
endogenous opioid peptide mechanisms.
Background
Shelley E. Taylor, Laura Cousino Klein, Brian P. Lewis, Tara L.
Gruenewald, Regan A. R. Gurung, and John A. Updegraff, Department o
f
Psychology, University of California, Los Angeles.
Laura Cousino Klein is now in the Department of Biobehavioral Health,
Pennsylvania State University; Brian Lewis is now in the Department o
f
Psychology, Syracuse University; and Regan Gurung is now in the
Department of Psychology, University of Wisconsin--Green Bay.
Support for preparation of this article was provided by National Science
Foundation Grant SBR 9905157, National Institute of Mental Health Grant
MH 056880, and the MacArthur Foundation’s SES and Health Network.
All of the authors except the first were supported by a National Institute o
f
Mental Health Training Grant in MH 15750 in health psychology at
various points throughout the preparation of this article. We are grateful to
Nancy Adler, David A. Armor, Lisa Aspinwall, John Cacioppo, Elissa
Epel, Alan Fiske, Gregg Gold, Melissa Hines, Margaret Kemeny, Jennife
r
Lerner, Sonja Lyubomirsky, Karen Matthews, Bruce McEwen, L. Anne
Peplau, Lien Pham, Inna Rivkin, Joan Silk, Robert Trivers, and Rosemary
Veniegas for their comments on previous versions of this article.
Correspondence concerning this article should be addressed to Shelley E.
Taylor, Department of Psychology, 1283 Franz Hall, University o
f
California, Los Angeles, Los Angeles, CA 90095-1563. Electronic mail
ma
y
be sent to ta
y
lors
@p
s
y
ch.ucla.edu.
The fight-or-flight response is generally regarded as the
prototypic human response to stress. First described by Walter
Cannon in 1932, the fight-or-flight response is characterized
physiologically by sympathetic nervous system activation that
innervates the adrenal medulla, producing a hormonal cascade that
results in the secretion of catecholamines, especially
norepinephrine and epinephrine, into the bloodstream. In addition
to its physiological concomitants, fight-or-flight has been adopted
as a metaphor for human behavioral responses to stress, and
whether a human (or animal) fights or flees in response to
sympathetic arousal is thought to depend on the nature of the
stressor. If the organism sizes up a threat or predator and
determines that it has a realistic chance of overcoming it, then
attack is likely. In circumstances in which the threat is perceived to
be more formidable, flight is more probable.
A coordinated biobehavioral stress response is believed to be at
the core of reactions to threats of all kinds, including attacks by
predators, assaults by members of the same species, dangerous
conditions such as fire, earthquake, tornado, or flooding, and other
threatening events. As such, an appropriate and modulated stress
response is at the core of survival. Through principles of natural
This article may not exactly replicate the final version published in the APA journal. It is not the copy of record.
412 TAYLOR ET AL.
selection, an organism whose response to stress was successful
would likely pass that response on to subsequent generations, and
the fight-or-flight response is thought to be such an evolved
response.
A little-known fact about the fight-or-flight response is that the
preponderance of research exploring its parameters has been
conducted on males, especially on male rats. Until recently, the
human literature was little better. Prior to 1995, women constituted
about 17% of participants in laboratory studies of physiological
and neuroendocrine responses to stress. In the last five years, the
gender balance has been somewhat redressed. We identified 200
studies of physiological and neuroendocrine responses to an acute
experimental stressor conducted between 1985 and the present,
utilizing 14,548 participants, 66% of whom were male, and 34% of
whom were female. Despite movement toward parity, the
inclusion of women in human stress studies remains heavily
dependent on the specific topic under investigation. For example,
women are overrepresented in studies of affiliative responses to
stress, and men are overrepresented in studies of neuroendocrine
responses to physical and mental challenges (Gruenewald, Taylor,
Klein, & Seeman, 1999).
Why have stress studies been so heavily based on males? The
justification for this bias is similar to the rationale for the
exclusion, until recently, of females from many clinical trials of
drugs, from research on treatments for major chronic diseases, and
from animal research on illness vulnerabilities. The rationale has
been that, because females have greater cyclical variation in
neuroendocrine responses (due to the reproductive cycle), their
data present a confusing and often uninterpretable pattern of
results. The fight-or-flight response may also be affected by
female cycling, and, as a result, evidence concerning a fight-or-
flight response in females has been inconsistent. But what if the
equivocal nature of the female data is not due solely to
neuroendocrine variation, but also to the fact that the female stress
response is not exclusively, nor even predominantly, fight-or-
flight?
Theoretical Model
An empirical gap such as the identified gender bias in stress
studies provides a striking opportunity to build theory. From a
metatheoretical perspective, we reasoned that a viable theoretical
framework for understanding female responses to stress may be
derived by making a few conservative evolutionary assumptions
and then building parallel and mutually constraining biological and
behavioral models.
We propose, first, that successful responses to stress have been
passed on to subsequent generations through principles of natural
selection: Those without successful responses to threat are
disproportionately unlikely to reach an age when reproduction is
possible. In the case of females, an additional assumption is that,
because females have typically borne a greater role in the care of
young offspring, responses to threat that were successfully passed
on would have been those that protected offspring as well as the
self. The female of the species makes a greater investment initially
in pregnancy and nursing, and typically plays the primary role in
activities designed to bring the offspring to maturity. High
maternal investment should lead to selection for female stress
responses that do not jeopardize the health of the female and her
offspring and that maximize the likelihood that they will survive.1
“Tending”, that is, quieting and caring for offspring and blending
into the environment may be effective for addressing a broad array
of threats. In contrast, fight responses on the part of females may
put themselves and their offspring in jeopardy, and flight behavior
on the part of females may be compromised by pregnancy and/or
the need to care for immature offspring. Thus, alternative
behavioral responses are likely to have evolved in females.
The protection of self and offspring is a complex and difficult
task in many threatening circumstances, and those who made
effective use of the social group would have been more successful
against many threats than those who did not. This assumption
leads to the prediction that females may selectively affiliate in
response to stress, which maximizes the likelihood that multiple
group members will protect both them and their offspring.
Accordingly, we suggest that the female stress response of tending
to offspring and affiliating with a social group is facilitated by the
process of “befriending,” which is the creation of networks of
associations that provide resources and protection for the female
and her offspring under conditions of stress.
We propose that the biobehavorial mechanism underlying the
tend-and-befriend pattern is the attachment/caregiving system, a
stress-related system that has been previously explored largely for
its role in maternal bonding and child development. In certain
respects, the female tending response under stressful conditions
may represent the counterpart of the infant attachment mechanism
that appears to be so critical for the development of normal
biological regulatory systems in offspring (Hofer, 1995).
Numerous investigations have explored the effects of the mother-
infant bond on infants’ emotional, social, and biological
development, but less literature has explored the counterpart
maternal mechanism, that is, what evokes tending behavior in the
mother. We will attempt to redress that oversight here. In addition,
we will suggest that the “befriending” pattern may have piggy-
backed onto the attachment/caregiving system and thus may be at
least partially regulated by the same biobehavioral systems
that regulate tending. From this analysis, it follows that
neuroendocrine mechanisms would have evolved to regulate these
response to stress, much as sympathetic activation is thought to
provide the physiological basis for the fight-or-flight response. We
propose that the neurobiological underpinnings of the
attachment/caregiving system (e.g. Pankesepp, 1998) provide a
foundation for this stress regulatory system; specifically, oxytocin
and endogenous opioid mechanisms may be at the core of the tend-
and-befriend response.
In essence, then, we are proposing the existence of an
endogenous stress regulatory system that has heretofore been
largely ignored in the biological and behavioral literatures on
stress, especially in humans. Accordingly, the empirical evaluation
of the viability of this theoretical position requires us to address
several questions: Is there neuroendocrine and behavioral evidence
for our contention that fight-or-flight is less characteristic of
female than male responses to stress? Is there a
neuroendocrinological basis for and behavioral evidence for
1 We note here that the term, “parental investment,” is a technical ter
m
from evolutionary theory, referring to time and effort devoted to offspring,
and not a judgmental evaluation suggesting that women care more about
children than men do, or a proscriptive term suggesting that women are o
r
must be the onl
y
p
arent who can take a
pp
ro
p
riate care of offs
p
rin
g
.
BIOBEHAVIOR RESPONSES TO STRESS IN FEMALES 413
Neuroendocrine Perspective on Fight
“tending” under stress in females, that is, nurturance and caring for
offspring under conditions of threat? Is there evidence of
differential affiliation by females under stress and a
neuroendocrine mechanism that may underlie it?
Consistent with the above analysis, neuroendocrine differences
between the sexes suggest that females are unlikely to show a
physical “fight” response to threat. Females largely lack androgens
and, in many species, androgens act to develop the male brain for
aggression either prenatally or post-natally, and then activate
aggressive behavior in specific threatening contexts (such as
responses to territorial establishment and defense).4 In humans,
gonadal hormones appear to influence the development of both
rough-and-tumble play and tendencies toward aggression, both of
which show moderate to large sex differences (Collaer & Hines,
1995).
To evaluate these hypotheses, we draw on several sources of
scientific evidence. We begin with evidence for gender
divergences in biological and behavioral responses to stress and
examine substantial neuroendocrine data from animal studies that
may account for these divergences. We use the animal literature
not to draw direct connections to human behavior, but because
animal studies enable researchers to test neuroendocrine
mechanisms directly, whereas such evidence is typically more
indirect in human studies. We then consider whether there are
neuroendocrine and behavioral parallels in the literature on human
and non-human primate responses to stress. Clearly, there are risks
in combining evidence from multiple sources that include
behavioral studies with humans and non-human primates and
neuroendocrine research from animal studies. However, any effort
to understand stress responses that ignores one or more of these
lines of evidence is potentially risky, because a comprehensive
biobehavioral account of stress response requires integration
across multiple sources of evidence. We will suggest appropriate
caveats in generalizing from one line of work to another when they
are warranted.
Although the exact role of testosterone in male attack behaviors
remains controversial, testosterone has been associated with
hostility and aggressive behavior in both human (e.g., Bergman &
Brismar, 1994; Olweus, Mattson, Schalling, & Low, 1980) and
animal studies (Lumia, Thorner, & McGinnis, 1994). In humans,
testosterone has been shown to increase with acute stress,
including high-intensity exercise (e.g., Cumming, Brunsting,
Strich, Ries, & Rebar, 1986; Mathur, Toriola, & Dada, 1986;
Wheeler et al., 1994) and psychological stress (although the
effects vary by the nature of the stressor and by individual
differences) (Christensen, Knussmann, & Couwenbergs, 1985;
Hellhammer, Hubert, & Schurmeyer, 1985; Williams et al., 1982).
Girdler, Jamner, and Shapiro (1997) found that, in men,
testosterone increased significantly with acute stress, and
testosterone reactivity to acute stressors was significantly
associated with level of hostility. Although human male aggression
is generally regarded as being under greater cortical control than is
true for lower order animals, a small but consistently positive
relation between self-reported hostility and testosterone has been
found in meta-analyses of aggression, as has a consistent
relationship between testosterone levels and assessments of
aggression made by others (Archer, 1990). Studies of captive
human male populations, including incarcerated felons and
psychiatric patients, also show positive relations between
testosterone and ratings of aggressive behavior (Benton, 1992).
Thus, testosterone may be a link by which sympathetic arousal is
channeled into hostility and interpersonal attack behavior among
males.
Females and the Fight-or-Flight Response
The basic neuroendocrine core of stress responses does not seem
to vary substantially between human males and females.2 Both
sexes experience a cascade of hormonal responses to threat that
appears to begin with the rapid release of oxytocin, vasopressin,
CRF (corticotropin-releasing factor), and possibly other hormones
produced in the paraventricular nucleus of the hypothalamus.3
Direct neural activation of the adrenal medulla triggers release of
the catecholamines, norepinephrine and epinephrine, and
concomitant sympathetic responses, as noted. Hypothalamic
release of CRF and other hormones stimulate the release of
adrenocorticotropin hormone (ACTH) from the anterior pituitary,
which, in turn, stimulates the adrenal cortex to release
corticosteroids, especially cortisol or corticosterone, depending
upon the species (Jezova, Skultetyova, Tokarev, Bakos, & Vigas,
1995; Sapolsky, 1992a). As such, both males and females are
mobilized to meet the short-term demands presented by stress.
The androgens, especially testosterone, are also implicated in
2 Both sexes show sympathetic arousal in response to the perception o
f
threat, with men showing somewhat stronger vascular responses, and
women somewhat stronger heart rate responses (Allen, Stoney, Owens, &
Matthews, 1993; Matthews & Stoney, 1988; Stoney, Davis, & Matthews,
1987; Stoney, Matthews, McDonald, & Johnson, 1988).
3 Different combinations of these hormones may be released in response
to different types of stressors. Vasopressin secretion, for example, is not
stimulated by a variety of stressors, although oxytocin release appears to be
a more consistent, though not universal, component of the neuroendocrine
response to stress (Jezova et al., 1995; Kalin et al., 1985).
4 The exact role that testosterone plays in aggression varies by species,
particularly whether it has organizational effects, activational effects, o
r
both (Archer, 1990; Beatty, 1984). In rodent species, for example,
aggression is organized perinatally by testosterone and requires androgren
for the activation of aggression in adulthood. Aggression in primates is
thought to be organized by testosterone prenatally, but is not necessarily
de
p
endent u
p
on andro
g
ens for later activation.
As already noted, however, a stress response geared toward
aggressing or fleeing may be somewhat adaptive for males, but it
may not address the different challenges faced by females,
especially those that arise from maternal investment in offspring.
The demands of pregnancy, nursing, and infant care render
females extremely vulnerable to external threats. Should a threat
present itself during this time, attacking a predator or fleeing by
the mother could render offspring fatally unprotected. Instead,
behaviors that involve getting offspring out of the way, retrieving
them from threatening circumstances, calming them down and
quieting them, protecting them from further threat, and
anticipating protective measures for stressors that are imminent
may increase the likelihood of survival of offspring. Given the
adaptiveness of such behaviors for females, neuroendocrine
mechanisms may have evolved to facilitate these behaviors and
inhibit behavioral tendencies to fight or flee.
414 TAYLOR ET AL.
Neuroendocrine Perspective on Flight
the development of rough-and-tumble play (Beatty, 1984; Collaer
& Hines, 1995). From an early age, one male acts as an evocative
stimulus for another male, inducing aggressive behavior (Maccoby
& Jacklin, 1974). In the human male, rough-and-tumble play is
believed to be organized prenatally by testosterone and androgens,
but because it occurs before puberty, it may not be dependent upon
testosterone for activation (see Beatty, 1984; Collaer & Hines,
1995, for reviews).
Although flight might appear to be the more probable first line
of defense of females to stressful events or threatening
circumstances, this response, too, may not be dominant in the
hierarchy of stress responses of females. Females who are
pregnant, nursing, or otherwise responsible for offspring may be
unable to flee without jeopardizing the health and safety of their
offspring. Although flight behavior among females is well-
documented in species whose offspring have the capability to flee
within hours after birth (e.g., ungulates such as deer or antelope),
in species where offspring remain immature for long periods of
time, flight by the female can require abandonment of offspring.
Females of most species spend a substantial proportion of their
fertile lives either pregnant, nursing, or raising young children, and
until recently, this was largely true of human females as well.
Given the very central role that these activities play in the
perpetuation of the species, stress responses that enabled the
female to simultaneously protect herself and her offspring are
likely to have resulted in more surviving offspring.
Human female aggressive responses are not organized by
testosterone or androgens either prenatally or post-natally, and the
typical low levels of those hormones in juvenile and adult females
means that predominantly male hormones are unlikely to be the
organizing factors that evoke a female fight response as they do in
males. The presence of either another male or another female does
not typically act as an evocative stimulus for human female attack
behavior, and human females do not engage in rough-and-tumble
play at the levels observed in males (Maccoby & Jacklin, 1974).5
In human males, there appears to be a link between sympathetic
reactivity and hostility, whereas women’s hostility is not reliably
linked to sympathetic arousal, suggesting that it is not a necessary
component of a fight-or-flight response (Girdler et al., 1997). If flight behavior in response to stress is indeed inhibited in
females, might there be a neuroendocrine basis for this inhibition?
McCarthy (1995) alludes to such a mechanism in her animal
studies of the behavioral effects of oxytocin and its modulation by
estrogen. In particular, she argues that animals in the natural
environment face a constant barrage of stress, and a continuous
stress response can have deleterious physiological effects.
Consequently, reactions that control stress responses have
physiological advantages. Oxytocin release may be such a
reaction. Oxytocin is a posterior pituitary hormone that is released
to a broad array of stressors by both males and females. It is
associated with parasympathetic (vagal) functioning, suggesting a
counterregulatory role in fear responses to stress (Dreifuss,
Dubois-Dauphin, Widmer, & Raggenbass, 1992; Sawchenko &
Swanson, 1982; Swanson & Sawchenko, 1980). In experimental
studies of the effects of exogenously-administered oxytocin with
rodents, oxytocin has been found to enhance sedation and
relaxation, reduce fearfulness, and decrease sympathetic activity,
patterns of responses that are antithetical to the fight-or-flight
response (Uvnas-Moberg, 1997). These effects appear to be
substantially more pronounced in female rats than in males for
several reasons. First, oxytocin release in response to stress
appears to be greater in females than in males (Jezova, Jurankova,
Mosnarova, Kriska, & Skultetyova, 1996). Second, androgens
have been shown to inhibit oxytocin release under conditions of
Female aggression is well-documented, of course. Our argument
is not that female aggression fails to occur, but that it is not
mediated by the sympathetic arousal-testosterone links that appear
to be implicated in fight responses for men. Extensive reviews of
the human aggression literature suggest that males may not be
inherently more aggressive than females, but that the patterns of
aggression between males and females differ (Bjorkqvist &
Niemela, 1992, for a review). Males are more likely to use
physical aggression in struggles for power within a hierarchy or to
defend territory against external enemies. Females reliably show
less physical aggression than males, but as much or more indirect
aggression (Holmstrom, 1992), that is, aggression in the form of
gossip, rumor-spreading, and enlisting the cooperation of a third
party in undermining an acquaintance. However, human females
still show lower levels of verbal aggression than males, although
this sex difference is smaller than that for physical aggression
(Eagly and Steffen, 1986). Overall, female aggressive responses
appear to be tied less to sympathetic arousal than male aggression,
being instead more cerebral in nature. For example, female
aggressive behavior may be more moderated by social norms and
learning, and by cultural, situational, and individual differences
(Bjorkqvist & Niemela, 1992; Eagly & Steffen, 1986).
The physical fight response is the most robust area of aggression
that shows higher levels for males than females, and these
differences are found in rodents, primates, and humans (Archer,
1990; Eagly & Steffen, 1986; Hyde, 1984). When female attack
behavior if observed, it appears to be confined to particular
circumstances. For example, female adult rats are aggressive
toward intruder (i.e., unfamiliar) males and females, primarily
when they are pregnant or nursing, behaviors which fall off rapidly
as pups mature (Adams, 1992). In addition, maternal attack
behavior toward potential predators that threaten offspring has
been well-documented (Adams, 1992; Brain, Haug, & Parmigiani,
1992; Sandnabba, 1992). In summary, female physical aggression
appears to be confined to situations requiring defense, rather than
to the broader array of threats that is found in males.6
5 Female rhesus monkeys exposed to testosterone in utero show
intermediate levels of rough-and-tumble play (greater than normal females
and less than males), underscoring the organizational effect that
testosterone appears to play prenatally for physical aggression at least some
primates (Goy, 1966, 1978; Phoenix, 1974a, 1974b, 1974c; Phoenix, Goy,
& Resko, 1968). There is also some evidence that aggression in extremely
aggressive women is associated with testosterone (Benton, 1992).
6 When female attack behavior is documented in rats, primates, or human
females, it is much more likely to be female-female aggression than female-
to-male aggression (Burbank, 1987; Fry, 1992) (except when threats to
offspring are involved); this female-to-female aggression appears to be
directed primarily against outsiders, such as intruder females in the rat, and
females outside one’s immediate social
g
rou
p
in
g
in
p
rimates and humans.
BIOBEHAVIOR RESPONSES TO STRESS IN FEMALES 415
stress (Jezova et al., 1996); and, third, the effects of oxytocin are
strongly modulated by estrogen (McCarthy, 1995).
The estrogen-enhanced anxiolytic properties of oxytocin (e.g.,
Windle, Shanks, Lightman, & Ingram, 1997) may explain the
consistent sex differences found in stress-related behavior among
rats. For example, in response to acute stress, female laboratory
rats show fewer behavioral indications of fear (e.g., freezing) than
males (e.g., Klein, Popke, & Grunberg, 1998), slower withdrawal
latencies to heat and mechanical stimuli, a longer tail-flick
response (Uvnas-Moberg, 1997), higher ambulation scores in
open-field tests, faster time to emerge from familiar into novel
territory, and a greater amount of exploration of novel territory
(Gray, 1971a, 1971b, as cited in Gray & Lalljee, 1974). The
exogenous administration of oxytocin in rats results in decreased
blood pressure (effects that last longer in females), decreased pain
sensitivity, and decreased corticosteroid levels, among other
findings also suggestive of a reduced stress response (Uvnas-
Moberg, 1997). Oxytocin is also known to promote maternal and
other forms of affiliative behavior which, McCarthy (1995) argues,
may be functional under stress, representing more adaptive
responses than extreme fear. Although McCarthy’s oxytocin-based
argument does not address flight behavior per se, its emphasis on
fear reduction for moderating the typical behavioral responses to
fear suggests that oxytocin may be implicated in the processes by
which fear in the rat is reduced, flight is avoided, and maternal and
other forms of affiliative behavior are increased under conditions
of threat (see McCarthy, 1995). These effects may be conditional
upon the development of a maternal bond between mother and
infant: Among mother-infant pairs where attachment bonds have
been formed, abandonment of infants under stress is rarely, if ever,
found (Keverne, Nevison, & Martel, 1999; Mendoza & Mason,
1999).
Whether and exactly how McCarthy’s argument can be applied
to the human situation remains to be seen. For example, although
female rats show fewer behavioral signs of anxiety than males, that
pattern may be reversed in non-human primates and humans,
although the data are ambiguous (Gray, 1971a, 1971b, as cited in
Gray & Lalljee, 1974).7 Nonetheless, as will shortly be described,
oxytocin in human females has been found to have similar effects
on anxiety, affiliation, and maternal behavior (e.g., Uvnas-
Moberg, 1997), and estrogen is associated with reduced anxiety in
human females (Gray, 1971a). In humans, oxytocin inhibits the
release of glucocorticoids, also suggesting an anxiolytic effect
(Chiodera et al., 1991). Consequently, the role of oxytocin in the
inhibition of “flight” responses merits continued cross-species
investigations.
In summary, we suggest that the flight response to stress may be
inhibited in females, and that such inhibition favors the survival of
the female and her offspring under conditions of stress. The
neuroendocrine underpinnings of this response may be oxytocin-
mediated.
Tending under Stress
Tending
As previously stated, the basic neuroendocrine core of stress
responses does not seem to vary substantially between human
males and females. In both sexes, threat triggers sympathetic-
adrenal-medullary (SAM) and hypothalamic-pituitary-adrenal
(HPA) activation, as well as the release of other neuroendocrine
responses that operate to prepare the organism to respond to the
stressor. How would a female responding to stress with
sympathetic arousal nonetheless quiet and calm down offspring?
We propose that the biobehavioral mechanism for the tending
process builds on the attachment/caregiving system. We explore
the hypothesis that the neuroendocrine mechanisms which may act
to modulate sympathetic arousal and HPA activation also act to
encourage tending to offspring under conditions of threat.
Attachment was originally conceived as a stress-related
biobehavioral system that is the mainstay of maternal bonding and
of child socialization (Bowlby, 1988). This largely innate
caregiving system is thought to be especially activated in response
to threat and to signs of offspring distress (such as “distress
vocalization”). The caregiving system has been heavily explored
through animal studies, with parallels in human developmental
investigations. A paradigm frequently adopted for empirical
investigations of mother-infant attachment/caregiving processes
involves separation, and under these circumstances, in a number of
species, both mothers and offspring show distress at separation.
For example, in a study of squirrel monkeys, a 30- to 60-minute
separation of mother and infant led to signs of distress and
increased plasma cortisol in both mothers and infants (Coe,
Mendoza, Smotherman, & Levine, 1978); upon being reunited, the
stress responses of both mother and infant declined (Mendoza,
Coe, Smotherman, Kaplan, & Levine, 1980). Meaney and
colleagues (e.g. Liu et al, 1997; Liu et al, in press; Frances, Diorio,
Liu, and Meaney, 1999) explicitly link tending responses to stress
and demonstrate consequent effects on the development of stress
regulatory systems. In one of their paradigms, infant rats are
removed from the nest, handled by a human experimenter, and
then returned to the nest. The immediate response of the mother is
intense licking and grooming and arched-back nursing which
provides the pup with immediate stimulation that nurtures and
soothes it; over the long-term, this maternal behavior results in
better regulation of somatic growth and neural development,
especially enhancing hippocampal synaptic development and
consequent spatial learning and memory in offspring. In certain
respects, the female tending response under stressful conditions
may represent the counterpart of the infant attachment and
separation distress signaling system (Hofer, 1995). Although
considerable research has explored the effects of the mother-infant
bond on infants’ development, less literature has explored the
counterpart mechanism in the mother. We here attempt to outline
the rudiments of what that response might be.
Oxytocin and endogenous opioid mechanisms may be at the
core of the tending response (Panksepp, Nelson, & Bekkedal,
1999). Evidence from a broad array of animal studies involving
rats, prairie voles, monkeys, and sheep show that central
administration of oxytocin reduces anxiety and has mildly sedative
properties in both males and females (e.g., Carter, Williams, Witt,
& Insel, 1992; Drago, Pederson, Caldwell, & Prange, 1986;
Fahrbach, Morrell, & Pfaff, 1985; McCarthy & Goldman, 1994;
McCarthy, Chung, Ogawa, Kow, & Pfaff, 1991; Uvnas-Moberg,
7 Women report more psychological distress in response to stressful
events than do men, but these self-reports do not necessarily parallel
physiological processes (e.g., Collins & Frankenhaeuser, 1978;
Frankenhaeuser, Dunne, & Lundberg, 1976).
416 TAYLOR ET AL.
1997; Witt, Carter, & Walton, 1990). As noted, this response
appears to be stronger in females than in males, and oxytocin may
play two roles with regard to the female stress response. It may
serve to both calm the female who is physiologically aroused by a
stressor and also to promote affiliative behaviors, including
maternal behavior toward offspring. For example, studies of ewes
have found that intracerebroventricular administration of oxytocin
stimulates maternal behavior (Kendrick, Keverne, & Baldwin,
1987; see also Kendrick et al., 1997). The resulting grooming and
touching that occurs in mother-infant contact may help quiet
infants. These effects appear to be bidirectional, inasmuch as
oxytocin enhances affiliative and affectionate contact which, in
turn, enhances the flow of oxytocin (Uvnas-Moberg, 1999).8 As
noted above, endogenous opioid mechanisms are also implicated
in maternal attachment processes. In rhesus monkeys,
administration of naloxone (an opioid antagonist) is associated
with less caregiving and protective behavior toward infants
(Martel, Nevison, Rayment, Simpson, & Keverne, 1993).
Similarly, administration of naltrexone, another opioid antagonist,
inhibits maternal behavior in sheep under experimental conditions
(Kendrick & Keverne, 1989). In rat studies, administration of
oxytocin antagonists diminishes the attractive qualities of
conditioned maternal cues and blocks behavioral indices of infant-
mother attachment (Panksepp et al., 1999).
A large number of animal studies suggest that this maternal
contact under stressful conditions has a wide array of immediate
benefits for offspring. Maternal touching among rats reduces
hypothalamic-pituitary-adrenal (HPA) alterations indicative of a
stress response in pups (i.e., corticotrophin-releasing factor) (Liu et
al., 1997; Pihoker, Owens, Kuhn, Schanberg, & Nemeroff, 1993;
Wang, Bartolome, & Schanberg, 1996). Separation from the
mother increases corticosterone secretion in rat pups, which is
reduced when the mother returns (Kuhn, Pauk, & Schanberg,
1990; Stanton, Gutierrez, & Levine, 1988). Studies of rhesus
monkeys have found that ventral contact between offspring and
mother following a threatening event promotes rapid decreases in
HPA activity and in sympathetic nervous system arousal (Gunnar,
Gonzalez, Goodlin, & Levine, 1981; Mendoza, Smotherman,
Miner, Kaplan, & Levine, 1978; Reite, Short, Seiler, & Pauley,
1981).
The estrogen-enhanced oxytocin responses documented in rats
and now explored in humans appear to be very strong. McCarthy
(1995), for example, refers to the effects of estrogen on oxytocin
as among the strongest known effects of estrogen. Uvnas-Moberg
(1997) found that, in rats, oxytocin-induced calming may last for
several weeks, suggesting that it is not continuously maintained by
oxytocin flow but, instead, is maintained by secondary changes
induced by the peptide. Moreover, these effects are not easily
blocked by oxytocin antagonists. The surprisingly robust, long
duration of these oxytocin-mediated effects suggests that they may
be exerted at the level of the genome (Uvnas-Moberg, 1997).
Thus, the oxytocin effect in females is potent, long-lasting, and
maintained by secondary changes, suggesting centrality and
importance, at least in animal studies.
Although studies with humans are less able to provide evidence
of underlying mechanisms, mother-infant attachment processes
have been found to have much the same benefits on human infants,
and as has been true in animal studies, oxytocin and endogenous
opioid mechanisms are thought to be at their core. Some of the
human evidence on the behavioral concomitants of oxytocin has
involved studies of nursing mothers, because oxytocin levels are
known to be high at this time. As in animal studies, nursing is
soothing to both mothers and infants. Blass (1997) reported that
consuming milk significantly reduced crying in human infants, and
sucking on a nipple is known to have a physiologically calming
effects in infants and can also reduce crying (Field & Goldson,
1984). Lower levels of sympathetic arousal have also been found
in lactating versus non-lactating women (Wiesenfeld, Malatesta,
Whitman, Grannose, & Vile, 1985). Women who are breastfeeding
are calmer and more social than matched-age women who are not
breastfeeding or pregnant, as determined by personality
inventories (Uvnas-Moberg, 1996); moreover, the levels of
oxytocin in these breastfeeding women correlated strongly with
the level of calm reported, and oxytocin pulsatility was
significantly correlated with self-reported sociability (Uvnas-
Moberg, 1996). Similar findings are reported by Adler, Cook,
Davidson, West, and Bancroft (1986). Altemus, Deuster, Galliven,
Carter, & Gold (1995) found that lactating women showed
suppressed hypothalamic-pituitary-adrenocortical responses to
stress, consistent with the animal literature showing reduced HPA
activity in response to oxytocin (see also Chiodera et al., 1991;
Lightman & Young, 1989). Dunn and Richards (1977) also
reported higher levels of maternal behavior among lactating versus
non-lactating mothers.
Until recently, it was difficult to examine the relation of
oxytocin to human social behavior except during lactation, in part
because of ethical issues involved with manipulating oxytocin
levels, and in part because there were no commercially-available
assays to measure oxytocin at the levels suspected to be implicated
in stress responses. Emerging evidence suggests that oxytocin is
associated with relaxation and interpersonal outcomes in non-
lactating women as well. For example, in a sample of nulliparous
women, Turner, Altemus, Enos, Cooper, and McGuinness (1999)
found that oxytocin levels increased in response to relaxation
massage, and decreased in response to sad emotions. Women who
reported fewer interpersonal problems of intrusiveness showed
greater increases in oxytocin in response to these sources of
stimulation. Maintaining oxytocin levels during sadness was
associated with lower anxiety in close relationships, and high basal
levels of oxytocin were associated with greater interpersonal
distress. In an experimental study with older women, Taylor,
Klein, Greendale, and Seeman (1999) found that higher levels of
oxytocin were associated with reduced cortisol responses to stress
and with faster HPA recovery following an acute stress laboratory
challenge.
As is true in animal studies, human studies show that nurturing
behaviors under conditions of stress benefit both mother and
offspring. Field and colleagues have shown that touching an infant
and carrying an infant close to the mother’s chest can soothe and
calm the infant (Field, Malphurs, Carraway, & Pelaez-Nogueras,
1996; Field, Schanberg, Davalos, & Malphurs, 1996). High levels
of physical affection and warmth between mother and child during
8 Relevant to this is a study of gender differences in responsivity to
touch in humans in response to the stress of hospitalization (Whitcher &
Fisher, 1979). Results revealed that, under stress, touch produced more
favorable affective, behavioral, and physiological (especially
cardiovascular) effects in females than was true for males, and touch was
actuall
y
ex
p
erienced as aversive b
y
males.
BIOBEHAVIOR RESPONSES TO STRESS IN FEMALES 417
stressful circumstances have been tied to normal HPA activation
profiles in response to stress in offspring (e.g., Flinn & England,
1997; Chorpita & Barlow, 1998; Hertsgaard, Gunnar, Erickson, &
Nachmias, 1995). In humans (as well as in non-human primates),
these processes appear to be mediated by mother-infant
attachment, with securely-attached offspring less likely to show
elevated cortisol in response to challenging circumstances (e.g.,
Gunnar, Brodersen, Krueger, & Rigatuso, 1996; Gunnar,
Brodersen, Nachmias, Buss, & Rigatuso, 1996; Nachmias, Gunnar,
Mangelsdorf, Parritz, & Buss, 1996).
Nurturing behavior under stressful conditions may not only
quiet and soothe offspring, but also have discernible effects on
health-related outcomes, directly affecting the likelihood that
offspring will survive and mature properly.9 For example, in
humans, inadequate physical maternal care has been tied to growth
retardation, social withdrawal, and poor interpersonal relatedness,
among other complications (e.g., Harlow, 1986; Shaffer &
Campbell, 1994). Premature human infants given a pacifier or
massage grow better, become calmer, and become more tolerant to
pain (Bernbaum, Pereira, Watkins, & Peckham, 1983; Field &
Goldson, 1984; Scafidi, Field, & Schanberg, 1993; Uvnas-Moberg,
Marchini, & Winberg, 1993). In experimental investigations with
humans, touch and massage have been found to increase immune
function, decrease pain, reduce subjective reports of stress, and
maintain normal growth in infants (Field, 1995, 1996; Ironson et
al., 1996; Scafidi & Field, 1996).10
If mothers, in particular, exhibit nurturing behavior under
conditions of stress, it should also be possible to see behavioral
evidence for this prediction in parenting behaviors. Such evidence
is provided by Repetti’s (Repetti, 1989, 1997) studies of the effects
of stressful workdays on parenting behavior. Repetti interviewed
both fathers and mothers about their workdays and their behaviors
at home on those days, and also interviewed children regarding
their experiences with their parents on those days. She found that
fathers who had experienced an interpersonally conflictual day at
work were more likely to be interpersonally conflictual in the
home in the evenings. Fathers who had had highly stressful
workdays, but not involving interpersonal conflict, were more
likely to withdraw from their families (Repetti, 1989). A very
different pattern was found for mothers. Specifically, women were
more nurturant and caring toward their children on their stressful
work days. In particular, on days when women reported that their
stress level at work had been the highest, their children reported
that their mothers had shown them more love and nurturance
(Repetti, 1997). A second study replicated these differences in
mothers’ and fathers’ responses to offspring under stress (Repetti,
2000).11
The underpinnings of the tending response appear to be
oxytocin-based initially, at least in rodent and animal species, and
possibly also in human females12; prolactin, endogenous opioids,
and social learning may be more important for sustaining the
tending response, once the behavior pattern has developed
(Panksepp, 1998). The extent to which the tending response is
hormonally regulated over the long term is unclear, however. Rat
studies show that tending responses under stress (e.g., pup
retrieval) lose their complete dependence upon hormonal
regulation relatively quickly, and are thought to be socially
maintained instead, in response to distress vocalizations (DeVries
& Villalba, 1999). Tending responses in human females also
appear to depend, in part, on characteristics of human infant cries,
and such qualities as pitch and tone convey often quite subtle
information to mothers about the urgency and nature of the
infant’s need (Bates, Freeland, & Lounsbury, 1979; Crowe &
Zeskind, 1992; Zeskind, 1980, 1987; Zeskind & Collins, 1987;
Zeskind, Sale, Maio, Huntington, & Weiseman, 1985). The human
female not only brings the possibility of social evocation by
offspring to stress situations, but a large neocortex as well, and so
tending behavior in human females may be oxytocin-based,
socially mediated, mediated by higher-order brain functions, or
some combination of these three processes.
In summary, whereas male responses to stress may be tied to
sympathetic arousal and to a fight-or-flight pattern that is at least,
in part, organized and activated via androgens, female stress
responses do not show these androgen links and instead, may be
tied, at least in part, to the release of oxytocin and its
biobehavioral links to caregiving behavior. Oxytocin is believed
not only to underlie attachment processes between mothers and
offspring, but it may also be implicated in other close social bonds.
We extend this analysis in the next section by arguing that female
responses to stress are also characterized by affiliation with social
groups because group living provides special benefits for females.
Befriending Among Females
Group living is generally regarded as an evolutionary adaptation
among many species that benefits both males and females
(Caporeal, 1997). Groups provide more eyes for the detection of
predators, and most predators are reluctant to attack potential prey
if they believe there are others who might come to that prey’s
rescue (Rubenstein, 1978; Janson, 1992). Moreover, groups can
create confusion in a predator. If a predator charges a large group,
the group may disband in many directions, which may confuse the
predator long enough to reduce the likelihood that any one
member of the group can be taken down. Group life, then, is
fundamental to primate existence, making it an important
evolutionary strategy by which primates have survived (Caporeal,
1997; Dunbar, 1996). As we have noted, female stress responses
have likely evolved in ways that not only protect the female
herself, but also protect her offspring. As such, group life is likely
9 Bowlby’s (1988) theory of attachment maintains that the formation o
f
an attachment bond between infant and mother (or a suitable substitute) is
essential for adequate socialization. For example, human play behavior and
exploration in early ages is heavily dependent upon physical proximity to a
caregiver with whom that infant has formed a strong bond (see Hazan &
Shaver, 1994).
10 It should be noted that touch (Panksepp et al., 1999) and smell
(Kendrick, Levy, & Keverne, 1992) have been implicated in animal studies
of maternal-infant attachment, and these same behaviors may be implicated
in human mother-infant attachment processes to some degree as well (e.g.,
Fleming, Steiner, & Corter, 1997).
11 There appears to be an upper limit on this phenomenon, inasmuch as
chronically stressed or distressed mothers are somewhat more likely to
show withdrawal behavior on especially stressed days, rather than increases
in affection (Repetti & Wood, 1997).
12 Oxytocin may have important effects on social learning and social
memory (de Wied, 1997; Popik, Vetulani, & Van Ree, 1992). For example,
low doses of oxytocin strengthen social memories and, as such, oxytocin
may play a role in learning and memory for social bonds, infant caregiving,
and friendshi
p
s.
418 TAYLOR ET AL.
to have been an especially important adaptation for females and
offspring, because of the limitations of fight-or-flight as a female
response to stress. Like human males, human females required
successful defense against external predators, such as tigers,
leopards, hyenas, packs of hunting dogs, and other primates. In
addition, human females have much to fear from human males, in
the form of rape, assault, homicide, and abuse of offspring.13 The
pairing of human females with human males may be, in part, an
evolutionary adaptation that protects females and offspring against
random assault by males. However, under some conditions, human
females also have reason to fear their own male partners. In North
America, estimates of the percentage of women who have been
assaulted by their partners range from 20% to 50% (Bray, 1994;
Goodman, Koss, Fitzgerald, Russo, & Keita, 1993; Koss,
Goodman, Browne, Fitzgerald, Keita, & Russo, 1994; Malamuth,
1998; Straus & Gelles, 1986), and statistical analyses of assault
and homicide data reveal that human females are most likely to be
assaulted or killed by their own partners (see Daly & Wilson,
1988; Daly, Wilson, & Weghorst, 1982). There is no reason to
believe that this is a particularly modern phenomenon. Thus,
evolved mechanisms of female survival likely protected against a
broad array of threats, including those from males of her own
species.
If the above reasoning is true, one would predict a strong
tendency among females to “affiliate” under conditions of stress.
There is animal data consistent with this analysis. Crowding has
been found to stress male rodents, but to calm female rodents, as
assessed by corticosteroid levels (specifically, spatial crowding is
problematic for males, whereas number of other animals present is
positively related to calming in females) (Brown, 1995; Brown &
Grunberg, 1995). McClintock (1998) has reported that female rats
housed together in five-female groupings live 40% longer than
females housed in isolation.14 Research on prairie voles, a
preferred species for studying behavioral concomitants of
oxytocin, has found that, under conditions of stress, female prairie
voles show selective preference for their same-sex cage
companions (DeVries & Carter, unpublished data, cited in Carter,
1998).
Human Evidence for Affiliation Under Stress
Research on human males and females shows that, under
conditions of stress, the desire to affiliate with others is
substantially more marked among females than among males. In
fact, it is one of the most robust gender differences in adult human
behavior, other than those directly tied to pregnancy and lactation,
and it is the primary gender difference in adult human behavioral
responses to stress (Belle, 1987; Luckow, Reifman, & McIntosh,
1998). In their analysis of gender differences in coping, Luckow et
al. (1998) found that the largest difference arose on “seeking and
using social support,” and the combined significance of their effect
was significant beyond the p < .0000001 level. Of the 26 studies
that tested for gender differences, one study showed no differences
and 25 favored women; there were no reversals (Luckow et al.,
1998). Indeed, so reliable is this effect that, following the early
studies on affiliation in response to stress by Schachter (1959),
most subsequent research on affiliation under stress used only
female participants.15
Nonetheless, some research has compared males’ and females’
responses to stress. Bull et al., (1972) found that exposure to noise
stress led to decreased liking among male participants, but greater
liking by females toward familiar others. Bell and Barnard (1977)
found that males prefer less social interaction in response to heat
or noise stress, whereas females preferred closer interpersonal
distance. Affiliation under stress, however, is not random (Bull et
al., 1972; Kenrick & Johnson, 1979; Schachter, 1959). Women’s
affiliative tendencies under stress are heavily to affiliate with other
women (Schachter, 1959). When given a choice to affiliate with an
unfamiliar male versus alone prior to a stressful experience,
women choose to wait alone (Lewis & Linder, 1999). In summary,
then, women are more likely than men to choose to affiliate in
response to a laboratory challenge, but affiliation appears to be
selectively with similar others, especially other women.
Across the entire life cycle, females are more likely to mobilize
social support, especially from other females, in times of stress.
They seek it out more, they receive more support, and they are
more satisfied with the support they receive. Adolescent girls
report more informal sources of support than do boys, and they are
more likely to turn to their same-sex peers for support than are
boys (e.g., Copeland & Hess, 1995; see Belle, 1987, for a review).
College student females report more available helpers and report
receiving more support than do males (e.g., Ptacek, Smith, &
Zanas, 1992; see Belle, 1987, for a review). Adult women
maintain more same-sex close relationships than do men, they
mobilize more social support in times of stress than do men, they
rely less heavily than do men on their spouses for social support,
they turn to female friends more often, they report more benefits
from contact with their female friends and relatives (although they
are also more vulnerable to network events as a cause of
psychological distress), and they provide more frequent and more
effective social support to others than do men (Belle, 1987;
McDonald & Korabik, 1991; Ogus, Greenglass, & Burke, 1990).
Although females give help to both males and females in their
support networks, they are more likely to seek help and social
support from other female relatives and female friends than from
males (Belle, 1987; Wethington, McLeod, & Kessler, 1987).16
Women are also more engaged in their social networks than are
men. They are significantly better at reporting most types of social
network events than men, such as major illnesses of children, and
they are more likely to report being involved if there is a crisis
event in the network (Wethington et al., 1987). In an extensive
study of social networks, Veroff, Kulka, and Douvan (1981)
reported that women were 30% more likely than men to have
13 Although abuse of children does not differ significantly by gender o
f
perpetrator (U.S. Department of Health & Human Services, 1999),
correcting for time spent with children yields considerably higher rates fo
r
men than women. Stepfather status is a particularly potent predictor o
f
abuse (Rosenthal, 1988; Daly and Wilson, 1996).
14 No males were included in this particular study.
15 The late Stanley Schachter maintained, in several contexts, that he had
not found affiliative behavior in men under stress and, consequently,
conducted his subsequent studies on affiliation using females only.
16 It should be noted that, although men are less likely to seek and give
social support than women, they are often recipients of social support, and
such support, especially from a female partner, close relative, or close
female friend, appears to be successful in reducing physiological arousal in
response to stress (e.g., Kirschbaum, Klauer, Filipp, & Hellhammer, 1995).
Similar findings emerge in the primate literature. Sapolsky reports that
males who are the recipients of grooming efforts by females have bette
r
p
h
y
siolo
g
ical functionin
g
(
Sa
p
olsk
y,
1994
)
.
BIOBEHAVIOR RESPONSES TO STRESS IN FEMALES 419
provided some type of support in response to network stressors,
including economic and work-related difficulties, interpersonal
problems, death, and negative health events. So consistent and
strong are these findings that theorists have argued for basic
gender differences in orientation toward others, with women
maintaining a collectivist orientation (Markus & Kitayama, 1991)
or connectedness (Clancy & Dollinger, 1993; Niedenthal & Beike,
1997; Kashima, Yamaguchi, Choi, Gelfand, & Yuki, 1995) and
males, a more individualistic orientation (Cross & Madson, 1997).
These findings appear to have some cross-cultural generalizability:
In their study of six cultures, Whiting and Whiting (1975) found
that women and girls seek more help from others and give more
help to others than men do, and Edwards (1993) found similar sex
differences across 12 cultures.
In stressful circumstances where resources are scarce, female
networks for child care and exchange of resources often emerge
and become very well developed. Large kin networks among
disadvantaged African-Americans, as well as the fictive kin
networks that often evolve when real kin are not available are
well-documented (Stack, 1975). Newman (1999) described the all-
female economic networks that impoverished Dominican women
develop, so as to protect themselves and their children when male
breadwinners are unemployed or leave the family. Studies of
Black families, White working class families, White ethnic
families, and low-income families of all races reveal the
importance of the instrumental assistance and emotional support
shared among female kin, friends, and neighbors, especially
around the tasks of child-rearing (Belle, 1987).17
The preceding analysis is not intended to suggest that males are
not benefitted by social group living or that they do not form social
groups in response to external threats or stress. But
anthropological accounts, as well as survey literature, suggest that
the functions of the groups that men and women form and/or turn
to under stress are somewhat different. In a broad array of cultures,
men have been observed to form groups for purposes of defense,
aggression, and war (Tiger, 1970). They tend toward larger social
groups than is true of women (Baumeister & Sommer, 1997), and
these groups are often organized around well-defined purposes or
tasks. Although men orient toward and invest in a large number of
social relationships, many of these emphasize hierarchies of status
and power, rather than intimate bonding (Baumeister & Sommer,
1997; Spain, 1992). Female groupings tend to be smaller, often
consisting of dyads or a few women, and although some such
groups are focused around tasks (such as food preparation, sewing,
or collective child care), these groups often have the establishment
and maintenance of socioemotional bonds at their core, a
characteristic less true of male groupings (Cross & Madson, 1997).
Women in women’s social groups show more affiliative behaviors,
including smiling, disclosure, attention to others, and ingratiation
(Baumeister & Sommer, 1997; Pearson, 1981), and they interact at
closer interaction distances than do men’s groups (Patterson &
Schaeffer, 1977).
A Neuroendocrine Perspective on Affiliation Under Stress
Studies of affiliative behaviors in animal studies suggest a
mechanism whereby enhanced social activity of females may
occur under conditions of stress. In particular, they suggest that
oxytocin reduces stress and enhances affiliation. For example,
social contact is enhanced, and aggression diminished, following
central oxytocin treatment in estrogen-treated female prairie voles
(Witt et al., 1990), and the exogenous administration of oxytocin
in rats causes an increase in social contact and in grooming
(Argiolas & Gessa, 1991; Carter, DeVries, & Getz, 1995; Witt,
Winslow, & Insel, 1992). With reference to humans, Carter (1998)
suggests that oxytocin may be at the core of many forms of social
attachment, including not only mother-infant attachments, but also
adult pair bonds and friendships (Drago et al., 1986; Farbach et al.,
1985; Pankesepp, 1998). Keverne et al. (1999) suggested that
female-to-female bonding may have piggybacked onto
maternal/infant bonding attachment processes. Consistent with
Keverne et al.’s (1999) hypothesis, research has reported that
animals prefer to spend time with animals in whose presence they
have experienced high brain oxytocin and endogenous opioid
activities in the past (Panksepp, 1998), suggesting that friendships
may be mediated by the same neurochemical systems that mediate
maternal urges. As is true of the maternal-infant caregiving
system, contact with a friend or a supportive other person during
stressful events downregulates sympathetic and neuroendocrine
responses to stress and facilitates recovery from the physiological
effects of acute stress (Christenfeld, Gerin, Lindon, Sanders,
Mathur, Deich, & Pickering, 1997; Fontana, Diegnan, Villeneuve,
& Lepore, 1999; Gerin, Milner, Chawla, et al., 1995; Gerin, Piper,
Levy, & Pickering, 1992; Glynn, Christenfeld, & Gerin, 1999;
Kamark, Manuck, & Jennings, 1990; Kirschbaum, Klauer, Filipp,
& Hellhammer,1995; Kors, Linden & Gerin, 1997; Lepore, Allen,
& Evans, 1993; Roy, Steptoe, & Kirschbaum, 1998; Sheffield, &
Carroll, 1994; Thorsteinsson, James, & Gregg, 1998). Both men
and women experience these stress regulatory benefits of social
support, but women disproportionately seek such contact, and the
stress-reducing benefits are more consistent when the support
provider is female rather than male (e.g. Gerin et al, 1995).
The enhanced desire for social contact that females demonstrate
17 Studies of human female networks suggest that matrilinear and
matrilocal societies are typically characterized by peaceful interfemale
relations (Glazer, 1992). When generations of related women and girls live
together all their lives and participate in cooperative work groups,
interfemale aggression is reported to be low (Benedict, 1934; Glazer, 1992;
Murphy & Murphy, 1974). Reliably, however, when women join
patriarchal extended families, interfemale aggression is considerably
higher, especially between in-laws. These findings are true both for human
social groupings and for primate social groupings (Glazer, 1992; Keverne
et al., 1999).
An intriguing study of hunting among women of the Agta Negrito o
f
Luzon (the Philippines) underscores the functions of networks of female
kin. Women’s hunting has largely been regarded as biologically
impractical, because hunting is assumed to be incompatible with the
obligations of maternal care of offspring (Dahlberg, 1981; Hiatt, 1970; Lee,
1979). Specifically, hunting forays are thought to impair women’s abilities
to nurse, care for, and carry children, and female odor itself may constitute
a handicap to effective hunting. However, studies of cultures where the
females do hunt suggest exceptions that prove the rule. Agta women
participate actively in hunting precisely because others are available to
provide child care responsibilities (Goodman, Griffin, Estioko-Griffin, &
Grove, 1985). When women were observed to hunt, they either brought
nursing children with them, or gave the child to their mothers or oldest
female siblings for care. Whereas men typically hunted alone, women
almost always hunted with dogs and/or in groups, often with other females,
especially sisters. Thus, proximity to hunting grounds, use of dogs, hunting
in groups, and cooperation in child care appear to be the key factors that
make it
p
ossible for A
g
ta female hunters to be successful.
420 TAYLOR ET AL.
under conditions of stress, relative to males, may also be
modulated by endogenous opioid mechanisms. Endogenous opioid
peptides are released during stress, and are believed to influence
social interaction (Benton, 1988; Jalowiec, Calcagnetti, &
Fanselow, 1989). Animal studies suggest that higher levels of
endogenous opioids are associated with higher levels of social
interaction and maternal behavior. For example, Martel et al.
(1993) found that administration of naloxone (an opioid
antagonist) in female rhesus monkeys reduced both maternal
behavior as well as social grooming of other females. Further
support for this hypothesis and for its possible differential
relevance for females is provided by an experimental investigation
of the effects of opioids on affiliative behavior in humans. Jamner,
Alberts, Leigh, and Klein (1998) found that administration of
naltrexone (a long-acting opioid antagonist) increased the amount
of time women spent alone, reduced the amount of time that they
spent with friends, and reduced the pleasantness of women’s social
interactions, as compared with men; in addition, women given
naltrexone initiated fewer social interactions than when they
received a placebo. Thus, endogenous opioids appear to play a role
in regulating social interactions, especially for women.
Endogenous opioids also moderate the release of other peptides in
the limbic system (e.g., oxytocin, vasopressin), as well as other
“stress-related” neurohormones, such as norepinephrine (Keverne
et al., 1999), and cortisol (Klein et al., 1998), which may
contribute to the sex differences observed in social behavior under
conditions of stress.
Advantages of Affiliation Under Stress
What are the advantages of social affiliation under stress, and
why do females to do it more? Why does female affiliation under
stress appear to be at least somewhat selectively with other
females? We reasoned that examining evidence from humans’
closest relatives, namely Old World non-human primates, may
provide some insights into the patterns and functions of female
affiliative responses to stress.18
Female-female networks of associations are common in non-
human primate societies. Among many Old World primates,
female coalitions and networks are formed early and are in place
when they are needed (Dunbar, 1996; Wallen & Tannenbaum,
1997). For example, in Gelada baboons, a mother and her two
daughters, or a sister, mother, and daughter may form an alliance
to provide support against threat. These long-term commitments
are solidified through grooming behavior, which may take up as
much as 10% to 20% of an animal’s time (Dunbar, 1996).
Intrasexual aggression within these matrilineal groupings is
reported to be low among females (although high among males),
while the reverse is true of affiliative behavior, with females
exhibiting more affiliative behaviors than males. These findings
appear to be similar across several species of monkeys and other
primates (Burbank, 1987; Glazer, 1992; Keverne et al., 1999).
Although these bonds and their functions appear to be stronger
when kin relationships are involved (Silk, 2000), unrelated females
in several primate species form similar bonds. Wallen and
Tannenbaum (1997) found that rhesus monkeys establish social
bonds with female peers, which provide security and promote the
maintenance of a matrilineal social system. Squirrel monkeys
typically associate with females of roughly the same age and spend
considerable time in close association (Baldwin, 1985; Mason &
Epple, 1969). In captive situations, female squirrel monkeys show
signs of distress in response to being separated from their cage
mates. In an experimental investigation, when female squirrel
monkeys were introduced to a novel environment, they showed
more distress when alone than when they experienced the new
environment in the company of their same-sex cage mates
(Hennessy, Mendoza, & Kaplan, 1982); these adverse reactions
were stronger for lactating mothers with infants than for non-
lactating females (Jordan, Hennessy, Gonzalez, & Levine, 1985).
The so-called “harem” structure that characterizes the breeding
patterns of many primates also suggests what some of the
protective functions of female groups may be (Wrangham, 1980).
The harem structure typically consists of a dominant male and
several females and their offspring. Primatologists have tended to
emphasize the benefits that the harem structure has for males,
enabling them to have all their eggs in one basket, so to speak, and
have somewhat overlooked the functions that the harem may
afford to females and offspring. Evidence suggests, however, that
the female harem may provide protection for females. With
reference to the Gelada baboons, Dunbar (1996) notes that
daughters mature into a harem grouping of females to join their
mothers, older sisters, aunts, and female cousins in a “coalition of
great intensity and loyalty…these alliances are formed at birth, the
product of being born to a particular mother” (p. 20). Mother-
daughter, sister-sister, and female friend grooming are all widely
documented and are described by Dunbar as “the cement that
holds alliances together,” (p. 20). Although males rarely groom
each other, adult females will often groom their close female
relations and friends in this fashion. Grooming does not occur at
random, but rather, takes place within the context of clearly
defined social relationships, most of which involve matrilinear
relatives or special friends (see also De Waal, 1996; Wrangham,
1980).
Grooming can be an indication of status as well as a form of
hygiene and an expression of friendship. The frequency with
which a female is groomed by others predicts how likely it is that
those others will come to her aid if she is attacked by members of
another harem, the male in her own harem, or an outside predator
(Dunbar, 1996; Wrangham, 1980). In his studies of rhesus
monkeys, Saroj Datta (cited in Dunbar, 1996, p. 25) noted that
whether a particular female is attacked may depend on such factors
as whether that female’s mother or other females with whom that
female has formed alliances are nearby. The probability of attack
is reduced if the targeted female is of high status or if her mother is
of high status, because there is greater potential to enlist the
support of other females to drive off a potential attacker.
Grooming behavior appears to be enhanced by oxytocin and may
be moderated by endogenous opioid mechanisms. For example,
among monkeys, naxolone has been found to reduce mothers’
grooming behavior toward their infants and toward other group
members (Martel et al., 1993).
These female groups may also provide protection for females
from their own males. On the one hand, the harem itself may be
protected by a dominant male who attempts to keep the females in
18 Old World primates include bonobos, gorillas, orangutans, and
chimpanzees (which are believed to be the closest relations of humans), as
well as certain monkeys, including baboons and macaques. New World
monkeys are the capuchins, muiriquis, and squirrel monkeys.
BIOBEHAVIOR RESPONSES TO STRESS IN FEMALES 421
line, in particular, preventing them from breeding with other
males. On the other hand, if he is overly aggressive or threatening
to a particular female, the chances that her female relatives will
come to her aid and threaten the male as a group is very high.
Dunbar (1996) describes an example of this protection:
The harem male’s attempts to ride herd on his females when they
stray too far from him often backfire. The luckless victim’s grooming
partners invariably come to her aid. Standing shoulder-to-shoulder,
they outface the male with outraged threats and furious barks of their
own. The male will usually back off, and walk huffily away,
endeavoring to maintain an air of ruffled dignity. However,
occasionally, the male will persist, feeling, perhaps, unusually
sensitive about his honor and security. This only leads to more of the
group’s females racing in to support their embattled sisters. The male
invariably ends up being chased ‘round the mountainside by his irate
females in an impressive display of sisterly solidarity (pp. 20-21).19
Similar accounts are found in De Waal (1996).
Female bonded groups also appear to be important for the
control of resources related to food (Silk, 2000; Wrangham, 1980).
Wrangham (1980) suggested that female bonded groups may have
evolved, in part, because of the competition that exists for high-
quality food patches under conditions of limited feeding sites.
Cooperative relationships among females may provide for the
sharing of information about food sites and also help supplant
others from preferred food patches (Silk, 2000; Wrangham, 1980).
Matrilocal primate groupings also provide opportunities for the
exchange of caretaking responsibilities under some circumstances
(Wrangham, 1980), and examples of one female taking care of the
offspring of another female appear commonly throughout the
primate literature (e.g., De Waal, 1996).
Studies of primates suggest that these groups of females and
their offspring may also be a critical mechanism by which juvenile
females gain experience in the tending of infants, enabling them to
observe the behaviors of other mothers. For example, studies with
rhesus macaque monkeys have reported that females who have not
yet given birth frequently help care for younger siblings (Keverne
et al., 1999). Research that has deprived monkeys of maternal or
social contact during the first eight months of life reveals
significant adverse effects on subsequent maternal care, including
infanticide and abuse; social contact and opportunities to provide
maternal care subsequently improves maternal care, but that care
does not approach that of feral mothers (e.g., Ruppenthal, Harlow,
Eisele, Harlow, & Suomi, 1974). When mothers and infants are
given opportunities to form bonds with each other, abandonment
of infants is rarely observed (Keverne et al., 1999; Mendoza &
Mason, 1999), but in captive-reared animals and other
circumstances when mother-infant bonds have not formed,
mothering behavior can be inadequate. This maternal behavior is
believed to be mediated, in part, by endogenous opioid
mechanisms. Related findings appear in studies of human
affiliative behavior (Jamner et al., 1998).
Although oxytocin and endogenous opioid mechanisms may be
important in affiliative and maternal behavior in primates and
humans, the important role of higher brain functioning must also
be noted. As Keverne et al. (1999) point out, the development of a
large neocortex in primates has allowed affiliative behavior and
maternal caregiving to take place without the hormonal regulation
prompted by pregnancy and parturition that elicits similar
behaviors in rats. Freeing behavior from exclusive neuroendocrine
control enables females to engage in affiliation and infant
caregiving through learning by modeling other females. These
points suggest an important socialization role for these all-female
social groupings. Indeed, Keverne et al. (1999) argue that, through
such learning, females provide social stability and group cohesion,
with their affiliative processes helping to maintain the continuity
of the group over successive generations.
Two caveats regarding the research on female networks in
primate groups are warranted. First, there are over 130 different
primate species, and there is substantial variability in the specifics
of female networks. For example, female associations are based on
kin in some primate social groupings, but on non-kin dominance
hierarchies in others. In most primate species, networks of females
are responsible for rearing offspring, but in titi monkeys, fathers
are responsible for the rearing of offspring, and titi females
actually show aversion to being left alone with their offspring
(Mendoza & Mason, 1999). While it would be unwise to draw
direct links from primate behavior to humans, it would be foolish
to claim that there is nothing to be learned from primate behavior,
merely because there is variability among primate species. Thus,
although these primate examples should be interpreted with
caution, they provide illustrations of the befriending patterns
common to many primates, including human females.
Second, the preceding analysis runs the risk of romanticizing the
networks that females create. It must be noted that these networks
are by no means stress-free, particularly non-kin female networks
(e.g., Silk, 2000). Studies of primates reveal how more dominant
females in the hierarchy may harass less dominant females, a
behavior that can have many adverse effects, including the
suppression of fertility (Abbott, Saltzman, Schultz-Darken, &
Smith, 1999; Shively, Laber-Laird, & Anton, 1997). A more
extreme response has been reported by Fossey (1983) in gorillas
and by Goodall (1986) in chimpanzees; in both species, dominant
females, together with their oldest female offspring, were found,
on occasion, to cannibalize the young of less dominant females. In
humans, interpersonal strain, conflict, and the potential for
misunderstanding and mistreatment are common in social groups,
and all-female groups are no exception. The networks that women
help create and may become enmeshed in are themselves sources
of stress, and women report that interpersonal stressors are the
most common and stressful types of stressors they experience
(Davis, Matthews, & Twamley, 1999). Nonetheless, on the whole,
these female networks may confer more benefits than harm.
Conclusions, Implications, and Limitations
We have proposed a theory of female responses to stress
characterized by a pattern termed “tend and befriend.”
Specifically, we proposed that women’s responses to stress are
characterized by patterns that involve caring for offspring under
stressful circumstances, joining social groups to reduce
vulnerability, and contributing to the development of social
groupings, especially those involving female networks, for the
exchange of resources and responsibilities. We have maintained
19 We are not suggesting that the female kin network evolved primarily
or even significantly to protect females against their own partners. It is,
however, likely that females have evolved mechanisms that protect the
m
and their offspring against jealous and suspicious partners, and female kin
networks may be one basis for so doing.
422 TAYLOR ET AL.
that aspects of these responses, both maternal and affiliative, may
have built on the biobehavioral attachment/caregiving system that
depends, in part, on oxytocin, estrogen, and endogenous opioid
mechanisms, among other neuroendocrine underpinnings. We
suggest that these patterns may have evolved according to
principles of natural selection and by virtue of differential parental
investment. We propose this theory as a biobehavioral alternative
to the flight-or flight response (Cannon, 1932), which has
dominated stress research of the last five decades and has been
disproportionately based on studies of males.
To evaluate our theory, we examined several empirical
literatures that provide convergent support. A neuroendocrine
literature on stress hormones and their relation to behavior derived
largely from studies with male rats and, to a lesser extent, on non-
human primates, suggests that the fight-or flight response may be
heavily tied to androgenic prenatal or post-natal organization of an
aggressive response to threat that is activated, in part, by
testosterone. A substantial neuroendocrine literature from animal
studies with females suggests, in contrast, that sympathetic and
HPA responses may be downregulated by oxytocin under stressful
circumstances, and that oxytocin, coupled with endogenous opioid
mechanisms and other sex-linked hormones, may foster maternal
and affiliative behavior in response to stress. The neuroendocrine
model links to a literature on humans suggesting that oxytocin and
endogenous opioid mechanisms may have similar maternal and
affiliative concomitants. Finally, literatures on both human and
non-human primates point to differential maternal and affiliative
activities among females, compared with males, and provides
evidence of a substantial female preference to affiliate under
stress. The tend-and befriend pattern may be maintained not only
by sex-linked neuroendocrine responses to stress but by social and
cultural roles as well.
Theoretical and Empirical Limitations
There are limitations in our analysis. We have combined
observations from stress literatures on rats, primates, and humans
in a manner that requires considerable leaps, both empirically and
inferentially. As noted, the reason for this unusual mode of
argumentation is because the neuroendocrine mechanisms are
addressed heavily by one literature (rodent), and the behavioral
responses to stress by two others (primate, human). It is impossible
to build a coherent and informed biobehavioral model that covers
what is known about female stress responses without drawing on
these diverse and largely unintegrated sources of evidence. This
need does not diminish the risks that such an analytic strategy
entails, however.
Some of the points in the preceding argument remain
conjectural. In particular, we have suggested that oxytocin and
endogenous opioids may play important roles in female responses
to stress, and it remains to be seen if these are as significant
players as we have suggested. It should be noted that the present
argument does not posit that oxytocin and endogenous opioids are
either necessary or sufficient bases for the behavioral responses
identified: We have argued that the “tending” response is
consistent with maternal investment in offspring, and maternal
behavior under stressful conditions is socially responsive to
distress vocalizations by offspring and is likely to be mediated by
cortical processes as well. The “befriending” pattern is one of the
most robust sex differences reported in the literature on adult
human behavior under stress (e.g., Belle, 1987; Luckow et al.,
1998), and it, too, may depend heavily on social and cortical
processes. At present, the potential roles of oxytocin and
endogenous opioids in mediating these patterns are sufficient to be
considered credible hypotheses, but they are not definitively
established.
Our analysis has included little consideration of the nature of the
stressor in moderating stress responses. Neuroendocrine responses
under stress are not uniform, but depend upon the stress stimulus
involved and other environmental conditions such as predictability
and chronicity of a stresssor (e.g., Glass & Singer, 1972; Sapolsky,
1992a; Staub, Tursky, & Schwartz, 1971). Under certain stressful
circumstances, we might find the tend-and-befriend pattern to be
quite descriptive of female responses to stress and, in other cases,
not descriptive (Jezova et al., 1996). In addition, because different
stressors elicit different patterns of stress hormones, oxytocin may
be involved in some kinds of stressful events, but not others (cf.
Sapolsky, 1992b; Kalin, Gibbs, Barksdale, Shelton, & Carnes,
1985).
Another limitation is that, at present, the model largely ignores
the very reason why stress responses in females have been so
understudied: cyclical variation. If the hypothesized
neuroendocrine underpinnings of female stress responses are
correct, then we might expect to see cyclical variation in these
responses, as well as a degree of dependence upon critical
reproductive-related events in a woman’s life, including onset of
puberty, pregnancy, lactation, and menopause. For example, if
estrogen is involved in the modulation of oxytocin-related
affiliative or maternal responses, the so-called tending/befriending
pattern may be stronger during the late luteal phase of cycle, as
opposed to the follicular phase, and diminished in post-
menopausal women. Consistent with these suggestions, in rhesus
monkeys, females are most social around the time of ovulation or
when they are treated with estrogen (Wallen & Tannenbaum,
1997), and oxytocin, in interaction with estrogen, has been
suggested as the mechanism by which this sociability occurs
(Carter, 1998). At present, however, more evidence is needed to
assess the validity of these hypotheses.
Social and Political Implications
The issue arises as to whether sex differences in human
behavior might not be better understood as differences in social
roles, rather than as evolved biobehavioral responses (Eagley and
Wood, 1999). For example, given substantial human behavioral
flexibility, one can question whether maternal investment in
offspring continues to be higher than that of fathers.20 In response,
we note that current differences between men and women in
parental investment do not matter so much as differential parental
investment during the period of time that stress responses
evolved. An evolutionary biobehavioral argument does not
constrain current human behavior, but neither is it necessarily
20 Survey data (Staines & Pleck, 1980; Burden & Googins, 1987; Ferber,
O’Farrell, & Allen, 1991), interview data (Hochschild, 1989), and analyses
of time use diaries (Robinson & Godbey, 1997) indicate that women
continue to bear the major responsibility for childcare, whether or not they
work for pay. These estimates suggest that mother’s childcare exceed
father’s childcare b
y
a factor of a
pp
roximatel
y
three to one
,
on avera
g
e.
BIOBEHAVIOR RESPONSES TO STRESS IN FEMALES 423
challenged by current human behavioral flexibility. We also note
that, although human social roles vary substantially across cultures
and may, in some cases, prescribe behavioral patterns for women
similar to the tend-and-befriend pattern, social roles alone are
unlikely to account for it. A social role position does not address
the cross-species similarities we have identified, nor can it account
for the underlying biological evidence for our position.
Nonetheless, it will be important for future research to detail the
parts of our biobehavioral model that are sensitive to
environmental input.
An analysis that posits biological bases for gender differences in
behavior raises important political concerns as well. Many women
feel, with some justification, that such models can be used to
justify patterns of discrimination and social oppression. To head
off any such effort, we emphatically point out that our analysis
makes no prescriptive assumptions about the social roles that
women occupy. Our analysis should not be construed to imply that
women should be mothers, will be good mothers, or will be better
parents than men by virtue of these mechanisms. Similarly, this
analysis should not be construed as evidence that women are
naturally more social than men or that they should shoulder
disproportionate responsibility for the ties and activities that create
and maintain the social fabric.
Other political concerns, however, may be based on false
assumptions about what biological underpinnings signify.
Biological analyses of human behavior are sometimes
misconstrued by social scientists as implying inflexibility or
inevitability in human behavior or as reductionist efforts that posit
behavioral uniformity. These perceptions constitute unwarranted
concerns about biological bases of behavior. Biology is not so
much destiny as it is a central tendency, but a central tendency that
influences and interacts with social, cultural, cognitive, and
emotional factors that results in substantial behavioral flexibility
(Crawford & Anderson, 1989; Tooby & Cosmides, 1992). The last
few decades of biological research have shown that, just as
biology affects behavior, so behavior affects biology, in ways
ranging from genetic expression to acute responses to stressful
circumstances. Rather than viewing social roles and biology as
alternative accounts of human behavior, a more productive
theoretical and empirical strategy will be to recognize how biology
and social roles are inextricably interwoven to account for the
remarkable flexibility of human behavior.
Implications For Future Research
The present analysis suggests several areas of research for future
investigation. We have presented a relatively primitive
neuroendocrine model, ascribing a heavy role to oxytocin,
endogenous opioid mechanisms, and estrogen. However, other
neurohormones such as serotonin (e.g., Bagdy & Arato, 1998;
Insel & Winslow, 1998; Knutson et al., 1998), prolactin (Insel,
1997; Panksepp, 1999), vasopressin (Panksepp et al., 1999),
dopamine (Berridge & Robinson, 1998; Kreek & Koob, 1998), and
norepinephrine (Kraemer, 1992; Panksepp et al., 1999) may also
be implicated in these pathways as well, in ways not yet fully
identified. Examination of the patterning of these neuroendocrine
responses in subsequent studies of both lower animals and humans
may help to clarify the neuroendocrine model further. Additional
behavioral sequelae of these patterns merit investigation, such as
suppression of sexual behavior in females under stress; the role of
stress responses in moderating gender differences in negative
affect, especially high levels of depression and anxiety in females
(Craske & Glover, in press; Frasch, Zetzsche, Steiger, &
Jirikowski 1995; Levine, Lyons, & Schatzberg, 1999); and the
neuroendocrine and behavioral underpinnings of eating behavior,
social withdrawal, and substance abuse under conditions of stress.
The range of female responses to stress, as outlined in this
paper, go beyond the acute fight-or-flight response that has been
argued to be the foundation of stress responses. Our analysis
suggests, instead, that aspects of a coordinated stress response are
structurally in place, which are then activated under conditions of
stress. This is not a particularly novel observation, inasmuch as
group living is precisely such a structural adaptation. The interplay
of such structural adaptations with acute stress conditions suggests
how primate and human stress responses may have assumed
increasingly complex forms as non-human primates and humans
encountered an ever more diverse array of stressors. Indeed, it
suggests a layering and patterning of means for responding to
stress that may provide a quite flexible set of reactions to a broad
array of situations and, as such, may be suited to managing chronic
stress, as well as acutely stressful conditions.
In this context, there may be value in thinking about the fight-
or-flight response as only part of a range of equally flexible male
responses. Fight-or-flight may have garnered disproportionate
attention in the scientific literature, because of the potent
behavioral responses it produces, such as aggression, and from the
risks it may create for men’s health, such as the early development
of cardiovascular disease (CVD). Other male responses to stress
may be meritorious of investigation. For example, some aspects of
the tend-and-befriend model may characterize male responses to
stress under some conditions as well. A more complete model
would also consider a broader range of male behavioral responses
to stress, such as affiliative behavior, protective behavior, and
social withdrawal; a broader array of stress-related disorders,
including substance abuse, accident rates, and homicide/suicide;
and a broader range of neuroendocrine responses, such as the roles
of serotonin, oxytocin, vasopressin, and endogenous opioid
mechanisms in mediating or moderating male responses to stress.
For example, some intriguing effects of vasopressin in male prairie
voles include guarding of territory, self defense, and guarding of
females in response to stress, and studies of the effects of oxytocin
in male rodents reveal effects on pair-bonding and affiliation (see
Carter, 1998, for a review). In short, much remains to be
discovered about men’s responses to stress as well.
Although our analysis has focused on human stress responses,
the present analysis may apply to some other mammalian species
as well. Under what circumstances should we see tending and
befriending responses to stress in females? Evidence of female
“tending” under conditions of stress may be especially pronounced
under conditions where there are long gestational periods of
offspring, when females spend a high proportion of their life in
activities related to pregnancy, nursing, and the rearing of
offspring, and in any species in which offspring remain
biologically immature for a long period of time. The “befriending”
response may be especially prevalent under conditions of resource
scarcity; in any species where females are smaller and less
powerful than males; when males are unavailable and/or there is a
high differential mortality between the sexes; when there is a high
rate of rape or attack of females; and when males commonly
424 TAYLOR ET AL.
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Received July 30, 1998
Revision received January 26, 2000
Accepted February 29, 2000
... Stress is the body's physiological response to a challenging and threatening event; the flight-or-flight response is activated via the sympathetic nervous system, which heightens activity in the amygdala (Sapolsky, 2003). Activating the flight-or-flight response has a substantial evolutionary benefit, as it is the body's response to many threatening stimuli (Lang, 1995) and may be a source of motivation to champion otherwise difficult situations (Taylor et al., 2000). Be that the fight-or-flight response has had evolutionary benefit; it can also have deleterious affect on the higher order thinking and ability to perform well academically (Cassady, 2004;Kirschbaum, Wolf, May, Wippich, & Hellhammer, 1996;Lazarus & Launier, 1978;Loewenstein & Lerner, 2003;Lesch, 2007). ...
... Unsurprising is the fact that student learning and development is negatively affected by high levels of stress and anxiety (Lesch, 2007). This is because individuals who report higher levels of stress and anxiety show signs that compromise their ability to make clear decisions void of misinterpretations, integrate information from various senses, express higher order thinking, and perform well academically (Taylor et al, 2000;Cassady, 2004;Kirschbaum et al., 1996;Lazarus & Launier, 1978;Lowenstein & Lerner, 2003;Lesch, 2007). As discussed, stress and anxiety may be what is impeding students' ability to develop critical thinking. ...
... The emerging field of neuroscience has provided new ways to investigate stress and anxiety and has validated specific treatments, such as behavioral regulation stratergies, that effectively combat heightened and prolonged states of stress and anxiety (Bush et al., 2000;Chiesa et al., 2011;Goldin, & Gross, 2010;Hutcherson et al., 2008;Kozasa et al., 2012;Lazar et al., 2005;Todd et al., 2012). The amygdala, the emotional processor of the brain, is where stress and anxiety starts (Lang, 1995;Sapolsky, 2003;Taylor et al., 2000). Other areas of the brain affected by a hyperactive amygdala include the: (1) hippocampus, which has a fundamental role in learning of tasks and translating memories from short to long term (Kim & Diamond, 2002;Kim et al., 2001), (2) hypothalamus, which acts as a translator between your brain and body using various hormones (LeDoux, 2003;Shallice & Burgess, 1991), and ...
Thesis
Full-text available
Integrative Inquiry is a training program that seeks to facilitate student learning and development based on seminal research in neuroscience and psychology, in turn the training program hopes to remedy some of the fracturing issues in post-secondary education. Bresciani, et al. reported that undergraduate and graduate students who had completed Integrative Inquiry, in its entirety, were able to decrease their stress and anxiety levels and increase their attention, emotion, and cognitive regulation, as well as their critical thinking dispositions. The present study sought to replicate Bresciani, et al. among doctoral students, and additionally, extended its analysis using document analysis. Results indicate that doctoral students were able to learn emotion regulation and cognitive regulation. However, doctoral students did not improve in their critical thinking dispositions or attention regulation, further, reported anxiety levels did not decrease. However, it is important to note that critical thinking dispositions were well above the national average prior to engaging in Integrative Inquiry leaving little room for improvement. Similarly, attention regulation did not improve but the pre-assessment revealed already high levels and thus left little room for improvement. Anxiety levels did not significantly decrease, however they did not increase as well, which suggests Integrative Inquiry was able to prevent heightened levels of anxiety during students first semester. A qualitative assessment uncovered other student learning including a better ability to articulate their subjective and objective mental processes, a shift in their relationship with time, and heightened connectedness with their environment and others. Taken together, these results suggest that INIQ is partially effective among doctoral students.
... However, it is still unclear how acute stress might impact prosocial behaviours. Two contrasting theoretical accounts propose that acute stress might result in either an increase (e.g., Tend-and-Befriend; Taylor et al., 2000) or a decrease (e.g., Fight-or-Flight;Cannon, 1939) in prosociality. Many research questions have been framed through this dichotomy in behavioural changes (either an increase or a decrease in sociality). ...
... We did not find evidence for differences in the effects of acute stress on men and women's prosocial behaviour. This is seemingly at odds with some theoretical accounts, such as the tend-and-befriend hypothesis (Taylor et al., 2000), that suggest gender differences in the response to acute stress, with women showing a higher propensity for affiliative behaviours, compared to men. However, it is unclear if economic games, as used in the current context, are necessarily the most appropriate means for testing affiliation. ...
... Given the focus of the 'tend and befriend' hypothesis on affiliation with kin or close others (Taylor et al., 2000), how does acute stress impact social behaviour towards closer others compared to strangers or charitable organisations? Previous studies suggest we tend to help closer others more under stress (e.g., Margittai et al., 2015). ...
Preprint
Prosocial behaviour is fundamental for our social togetherness. Yet, how acute stress, a common everyday occurrence, influences our behaviours towards one another is still unclear. In this systematic review and meta-analysis, we aimed to quantitatively investigate the effect of experimentally induced acute stress on prosocial behaviours in economic games. We also probed possible moderators to explain differences in findings. We included 23 studies, 77 individual effects, and 2197 participants in the meta-analysis and found no overall differences between stress and control groups in prosocial behaviours (SMD=-0.04), or costly punishment (SMD=-0.11). While we found significant heterogeneity in the reported research findings, there were no moderating effects of participants’ gender/sex, paradigm design-choices, and the type of stressor did not play a role in explaining divergent effects. The results of this meta-analysis suggest that there is currently no clear answer to the question of whether or not stress increases or decreases prosociality. We highlight important open questions and suggest where the field should go next.
... If cognition and threat have co-evolved together and if cognition and cooperation have also co-evolved together, it seems relevant to think that cognition, cooperation and threat are intimately linked, and that cooperation plays a major role in response to threat situations. Of interest, tend-andbefriend theoretical model originally developed by Taylor et al. (Taylor et al., 2000) seems particularly in line with these assumptions. This evolutionary model describes two types of behavior exhibited by organisms in response to threat: protection of offspring (tending) and seeking out their social group for mutual defense (befriending). ...
... But what if others were a relevant resource for survival? Befriending behaviors (in reference to tend-andbefriend model, Taylor, 2006;Taylor et al., 2000) in animal seems to be quite relevant to reduce probability of being hurt under threat, anxiety and individual cost in defensive actions (Caro, 2005). It is very likely that mechanisms allowing for tend-and-befriend defensive reactions have been selected by evolution (Taylor & Master, 2011). ...
Thesis
Individual reactions to threat are very often thought as individualistic and antisocial. However, more than fifty years of work in sociology and social psychology indicate that humans favor social strategies when confronted with threat. Indeed, cases of cooperation and mutual aid are often reported in the literature on disasters. To implement such strategies, psychological mechanisms that allow us to process social signals conveyed by others in order to act with them must be in place and these mechanisms must be maintained and even optimized in situations of intense anxiety. Understanding how danger reconfigures how we perceive our social environment and how we represent others and their actions, as well as the incentives of such strategies, is an important theoretical challenge. To tackle this issue, we led 3 studies. In the first one, we validated a within-subject method to induce anxiety in a sustained manner: the threat-of-scream paradigm, which consists in alternating blocks in which participants are at risk of hearing aversive distress screams at any time (threat blocks) with blocks in which they are not exposed to aversive stimuli at all (safe blocks). In a second study, we used this procedure to investigate how co-representation of action (i.e. the ability to automatically integrate the actions of other individuals into our own action plans to facilitate action coordination) is impacted under threat. Results showed that co-representation (assessed by measuring the magnitude of the classical Social Simon Effect) is maintained under threat contexts, and seems to be particularly boosted when participants are exposed to danger near safe partners. Our results suggest that the potential function of co-representing others’ actions could be to promote social strategies essential for one’s own survival. Finally, the third study addressed how facial displays of fear are perceived under threat. Indeed, depending on their associated gaze direction, they can either be appraised as signaling the presence of a potential threat in the surrounding environment (averted gaze), or as a signal of distress and potential need of help (direct gaze). Using a categorization task, we investigated if danger-related or distress-related signals were prioritized under the threat-of-scream procedure. We observed that the appraisal of danger-related signals transmitted by facial displays of fear is increased under threat contexts, with no impact on the appraisal of distress signals. Altogether, our results suggest that while social strategies are maintained under threat, they might be sustained by self-preservatives motives.
... Food intolerances can be described as any form of food sensitivity that does not involve an immunological mechanism. They can be classified according to their mechanism e.g., enzymatic, pharmacological or undefined [23,24], or alternatively can be defined in terms of the reactions they elicit e.g., metabolic food disorders, anaphylactoid reactions or idiosyncratic reactions [25]. Food intolerances usually produce less severe symptoms than food allergies, and affected individuals can usually tolerate some of the offending food in their diets. ...
... Reactions are due to an inherited deficiency of the enzyme, erythrocyte glucose-6-phosphate dehydrogenase. Most metabolic food disorders are genetically acquired and both lactose intolerance and favism occur at much higher frequencies in certain ethnic groups [25]. Anaphylactoid reactions have symptoms similar to those of anaphylaxis, but are triggered instead by non-immunological mechanisms, which directly lead to the release of chemical mediators from mast cells. ...
Article
Full-text available
Worldwide, monosodium glutamate is utilized as a flavor enhancer and is composed of essential amino acids for nutrition. Numerous health issues are thought to be linked to monosodium glutamate. Studies have demonstrated that monosodium glutamate has harmful side effects, notably in animals, such as the development of obesity and diabetes as well as hepatotoxic, neurotoxic, and genotoxic consequences. According to several accounts, human subjects were becoming more ravenous, eating more, and becoming obese. Only a few human studies have been done to examine the potential genotoxic, neurotoxic, and hepatotoxic consequences of monosodium glutamate. Exploring the molecular and metabolic mechanisms relating to monosodium glutamate will need a lot of investigation.
... In some instances, women in particular may respond to stressful environments as "tendand-befriend" rather than "fight-or-flight" to serve as a preventative buffer and network to on whom to rely when faced with stressful encounters (Taylor et al., 2000). Friends may also provide tangible support particularly as they may be more attuned to their friend's experiences of stress and/or trauma, effectively being "well-placed to provide unsolicited [tangible] social support" such as gift-giving, preparing meals, and sharing information when such things were not necessarily requested (Sias & Bartoo, 2007, p. 461). ...
Article
Emerging adults (EAs) experience many changes throughout this life-stage, characterized by self-focus, identity explorations, instability, in-betweenness, and possibilities of optimism (Arnett, 2014). As EAs transition from home of origin into independence, they may place more reliance on social networks apart from their family of origin (e.g., friends, Rawlins, 2009). Yet, chronically ill EAs may experience complications due to the biographical disruption, or interference of expectations in one’s life (Bury, 1982), particularly given that chronic illness is typically viewed as an elderly-related issue rather than occurring with youth (Kundrat & Nussbaum, 2003). Through transitions in the EA life-stage, EAs with chronic illness may forgo sharing chronic illness-relation information or withhold expressed desire for social support to appear more “normal” to fit in with their peers (Spencer et al., 2019). Thus, I centered the present study in Petronio’s (2002) Communication Privacy Management (CPM) theory to understand how EAs interact and negotiate (non)disclosure of chronic illness-related information with a friend. In the present interpretive and qualitative study, I analyzed and described how EAs interacted and negotiated the process of (non)disclosure of their chronic illness-related information with a friend. Data were 15 in-depth interviews and 15 book cover images to represent the experiences of EAs with chronic illness. In the results, I describe and explain how participants (a) engaged criteria for disclosure and identified the confidants of their disclosure, (b) created boundary rules around their chronic illness-related information, (c) perceived their friends’ role/non-role in chronic illness management, and (d) made sense of their chronic illness-related information management processes. I contribute four theoretical insights regarding CPM: (a) expanding confidant typology, (b) deconstructing disclosure criteria, (c) demonstrating dialectical tensions of private information disclosure, and (d) developing CPM concepts through metaphorical insights. I also offer two main practical implications: (a) creating a resource for EAs with chronic illness and (b) offering a strategy for arts-based therapeutic practice for those working with EAs experiencing biographic disruption. Advisor: Dawn O. Braithwaite
... Consoante com o estudo de referência, desenvolvido por Taylor et al., (2000), sobre a relação entre amizades e estresse descobriu-se que o gênero feminino reage ao estresse de forma diferente do gênero masculino, devido às diferentes proporções de hormônios -principalmente a ocitocina -liberados na corrente sanguínea. ...
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A presente dissertação propõe-se a analisar os fatores associados aos Transtornos Mentais Comuns em estudantes universitários de graduação nos campi da Universidade Federal da Bahia localizados na cidade de Salvador - BA, no ano de 2021. Logo, trata-se de uma pesquisa quantitativa, de corte transversal, do tipo analítico exploratório, realizada com estudantes da graduação dos gêneros feminino e masculino, com idade igual ou maior a 18 anos, matriculados regularmente em todos os cursos dos turnos: matutino, vespertino, noturno e integral. Assim sendo, a dinâmica do processo de investigação para a coleta dos dados consistiu na aplicação de questionários validados e autoaplicáveis em ambiente virtual: Questionário Socioeconômico-demográfico (QSD), Self-Reporting Questionnaire (SRQ-20) e o Questionário de Vivência Acadêmica em sua versão reduzida (QVA-r). Os dados foram submetidos à análise quantitativa utilizando-se o software Statistical Package for Social Sciences - SPSS, em sua versão 20.0, para o sistema operacional Windows. Dessa forma, realizou-se a análise descritiva do perfil epidemiológico das características demográficas, socioeconômicas, do estilo de vida dos estudantes universitários e das condições de infraestrutura, relações interpessoais e do processo de ensino-aprendizagem da referida instituição de ensino superior. Também foram calculadas as Razões de Prevalência da variável dependente e independente e os respectivos intervalos de confiança de 95%. Aplicou-se o Teste t de amostra independente para diferença entre médias, o Teste do Qui-Quadrado de Pearson e o Teste Exato de Fisher, a considerar o nível de significância de 5% (p ≤ 0,05) para avaliar a associação estatisticamente significante. Como resultados, participaram deste estudo 509 graduandos, sendo 367 (71,2%) do gênero feminino e 142 (27,9%) do gênero masculino, com idade média de 24,06 anos (DP = 6,566). Ademais, constatou-se uma prevalência para a suspeição de Transtornos Mentais Comuns (pontuação no SRQ-20 ≥ 7) de 78,6% da amostra, observada com maior percentual em estudantes do gênero feminino. Os resultados evidenciam, ainda, que ser do gênero feminino (p < 0,01), com cor/raça não-branca (p = 0,02), estado civil solteira (p = 0,01), sem apoio da Universidade frente às adversidades (p < 0,01) e que não considera a Universidade um ambiente acolhedor (p < 0,01) estiveram estatisticamente associados à maior ocorrência de Transtornos Mentais Comuns na amostra. Diante do descrito, discute-se a necessidade de novas investigações que complementem e aprofundem as questões, problemas e achados aqui apresentados e discutidos. Além disso, aponta-se para a necessidade de ações de cunho coletivo, tanto por parte dos gestores universitários quanto das entidades estudantis, bem como condutas institucionais, estratégias de cuidado em saúde mental e assistência intersetorial que proporcionem o bem-estar biopsicossocial dos discentes e a eficácia no estímulo de uma cultura institucional que valorize vivências acadêmicas mais saudáveis, humanas e solidárias no ambiente universitário.
... 89 This is also in line with the notion that women are more sensitive to interpersonal stressors than men, 90 and that social conflicts may hamper the ability to recruit social support, an important coping mechanism, particularly for women. 91,92 This interpretation, nevertheless, should be regarded with cautious considering the relatively young age of our participants, an age at which social responsibilities are potentially limited. Also related to the age of our participants, at their age many of them were still students, a population that might be particularly sensitive to social conflicts and to the effect of interpersonal stress, 16,19,93 and at the same time might be less sensitive to work-related stress. ...
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Background Chronic stress is a highly prevalent condition that may stem from different sources and can substantially impact physiology and behavior, potentially leading to impaired mental and physical health. Multiple physiological and behavioral lifestyle features can now be recorded unobtrusively in daily-life using wearable sensors. The aim of the current study was to identify a distinct set of physiological and behavioral lifestyle features that are associated with elevated levels of chronic stress across different stress sources. Methods For that, 140 healthy female participants completed the Trier inventory for chronic stress (TICS) before wearing the Fitbit Charge3 sensor for seven consecutive days while maintaining their daily routine. Physiological and lifestyle features that were extracted from sensor data, alongside demographic features, were used to predict high versus low chronic stress with support vector machine classifiers, applying out-of-sample model testing. Results The model achieved 79% classification accuracy for chronic stress from a social tension source. A mixture of physiological (resting heart-rate, heart-rate circadian characteristics), lifestyle (steps count, sleep onset and sleep regularity) and non-sensor demographic features (smoking status) contributed to this classification. Conclusion As wearable technologies continue to rapidly evolve, integration of daily-life indicators could improve our understanding of chronic stress and its impact of physiology and behavior.
... Benenson (2021) raised perhaps the most foundational question: how do female peers help one another's reproductive success? Although it is often taken as an assumption that same-sex peers provide fitness-enhancing benefits (Taylor et al., 2000), few investigations demonstrate the tangible mechanisms by which women contribute to one another's inclusive fitness. As Benenson noted, same-aged unrelated women would often be struggling to provide and care for their own children. ...
... Stress response depends on the context, its perception, and individual and social factors. For example, the "female" stress response is described as a "tend-and-befriend" reaction(Taylor et al., 2000; for more details, seeSeidel et al., 2013). ...
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Thanks to improvements in living standards and health behavior as well as medical progress since the second half of the twentieth century, old age has become a life phase in its own right. This phase usually begins by the transition from working life to retirement (Kohli, 2000). Both the chance of reaching retirement and the life expectancy after retirement have increased significantly (Eisenmenger & Emmerling, 2011). The post-work phase spans several decades for many people now. In addition, people who retire are considerably healthier and more independent than their peers of earlier birth cohorts (Crimmins, 2004). The expansion of this phase of life has been accompanied by a differentiation of older people in terms of health and independence: healthy and active people experience this phase, as do people in need of help and care. This fact is considered by distinguishing between old and very old people (Baltes, 2007). Characteristics of old age are absence of non-compensable health restrictions, self-determination of various activities (e.g., traveling, hobbies, voluntary work), and strong social integration. Overall, the demands of old age can be coped well in this phase. Very old age is characterized by an increase in physical and cognitive losses and diseases, and a decrease in the abilities and possibilities of compensating for deficits (Baltes, 1997; Baltes & Smith, 2003).
Purpose The purpose of this study is to utilize social cognitive theory to investigate how social comparison orientations, individual cognitive, and environmental factors influence females' decisions to pursue self-employment in the United Arab Emirates In doing so, the authors explore how the entrepreneurial self-efficacy of Emirati women also influences individuals towards entrepreneurship. Design/methodology/approach Using a survey instrument administered in both English and Arabic, data were collected from one hundred and three (103) employed Emirati women and eighty-four (84) self-employed Emirati women who were taking part in workshops conducted by the Dubai Chamber of Commerce. Findings The results from the study suggest that the social environment is a contributing factor toward self-employment, with higher levels of social comparison orientation increasing the likelihood of Emirati women being self-employed. Consistent with prior research, the authors also find that internal cognitive factors also play a significant role, with Emirati women possessing higher levels of entrepreneurial self-efficacy and having a higher likelihood of being self-employed. Originality/value This is one of the few studies aimed at exploring the role of social comparison orientation as a factor in motivating females towards entrepreneurship in the Middle East and North African (MENA) region.
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[examines] developmental trends in the new research on human female aggression, considering the present stage of knowledge about, and discussing the reasons for, its various forms in different cultures as well as its occurrence during diverse life stages and situations / since much of this research has been an attempt to describe in what way such aggression varies from its male counterpart, attention is necessarily drawn here to the question of differences between the sexes female aggression: definition and forms / the "male" perspective / the danger of ethnocentrism / the problem of methodology / recent studies: methodological and cultural change / are males more aggressive than females (PsycINFO Database Record (c) 2012 APA, all rights reserved)