Abnormal, abusive, and stress-related behaviors in baboon mothers

Abnormal, Abusive, and Stress-Related Behaviors in Baboon Mothers Linda Brent, Tina Koban, and Stephanie Ramirez Background: Psychiatric disturbances during pregnancy and the postpartum period are especially serious, given the negative effects on the mother as well as the child. Understanding the causes of such disturbances has been difficult owing to the complexity of psychological, social, experiential, biological, and genetic factors involved. Methods: To determine the potential utility of a nonhuman primate model for the study of postpartum disorders, the pathologic and stress-related behavior of 62 female baboons living in social groups was studied during pregnancy and after the birth of an infant. Results: The prevalence of abnormal behavior and selfdirected scratching (a measure of stress response) was higher after birth of the infant. Subjects displayed a significantly higher frequency per hour of these behaviors postpartum, which increased over 8 weeks. Abusive behaviors toward the infant were common, occurring in 55% of the subjects. Mothers with low dominance rank, who usually have lower levels of social support, had higher levels of abusive behavior during the postpartum period. Conclusions: Baboons show variation in measurable behaviors related to stress and abnormal functioning during the pre- and postpartum periods, indicating that a nonhuman primate model may be useful in the study of factors affecting postpartum psychiatric disorders and infant abuse. Biol Psychiatry 2002;52:1047–1056 © 2002 Society of Biological Psychiatry Key Words: Postpartum, baboon, psychiatric disorder, abuse, stress, abnormal

Introduction

P

sychiatric disturbances are more likely in women of childbearing age than later in life (Kessler et al 1994). The postpartum period in particular is associated with both an increased risk of onset and heightened vulnerability of relapse for mood and anxiety disorders (Altshuler et al From the Department of Laboratory Animal Medicine and Southwest National Primate Research Center, Southwest Foundation for Biomedical Research, San Antonio, Texas. Address reprint requests to Linda Brent, PhD, Southwest Foundation for Biomedical Research, Department of Laboratory Animal Medicine, P.O. Box 760549, San Antonio TX 78245. Received May 7, 2002; revised July 17, 2002; accepted July 23, 2002.

© 2002 Society of Biological Psychiatry

1998). Depressive disorders after the birth of a child are usually divided into three categories: transient mood disturbances, or “postpartum blues” (Pitt 1973), syndromal postpartum depression (Altshuler et al 1998; O’Hara 1997; O’Hara et al 1990; Stowe and Nemeroff 1995), and postpartum psychosis (Brockington et al 1981; Pedersen 1999). The incidence of psychosis is over 20 times greater during the first month postpartum than at other times before or after childbirth (Kendell et al 1987). Although less research has been conducted on postpartum anxiety disorders, current findings indicate that panic disorders may improve during pregnancy and worsen during the postpartum period, whereas obsessive-compulsive disorders worsen during pregnancy and the puerperium (Altshuler et al 1998; Shear and Mammen 1995). Women may develop other psychiatric problems after the birth of their infant, including posttraumatic stress disorder, loss of libido, mother–infant relationship disorders, and delusions (Brockington 1996; Lanczik et al 1999; Saintfort and Stern 2000). A past history of psychiatric disturbance, and depressive symptoms in particular, are often related to postpartum disorders (Kendell et al 1987; O’Hara et al 1991). The onset of psychiatric illness in the postpartum period is correlated with an increased risk of future episodes (Cooper and Murray 1995; Robling et al 2000). As well as affecting the future well-being of the mother, postpartum disturbances can have measurable negative affects on the relationship between the mother and infant, and even the intellectual and social development of the infant (Buist 1998; Galler et al 2000; Murray and Cooper 1997). Cognitive differences have been found in children of depressed mothers, and these effects may be moderated by the mother’s education level and the child’s gender and birth weight (Hay 1997). In extreme cases, the mother may harm or even kill her child as a result of severe postnatal psychiatric problems (Adshead et al 2000; Marks and Kumar 1993). Even if they do not act on their impulses, depressed mothers have a much higher incidence than control subjects of thoughts of harming their infants (Jennings et al 1999), and those with obsessive-compulsive disorders usually have intrusive thoughts of harming the child (Sichel et al 1993). 0006-3223/02/$22.00 PII S0006-3223(02)01540-8

1048

BIOL PSYCHIATRY 2002;52:1047–1056

Although abusive parents often show signs of psychopathology, such as depression, neuroses, and schizophrenia, parents who abuse a child do not always suffer from a distinct psychiatric disorder. Abusive parents may be quantitatively, not qualitatively, different from nonabusers (Prodgers 1984; Rogers 1983). Parental abuse is frequently related to the individual having experienced neglect or abuse as a child and having lower social support (Rogers 1983; Smith and Hanson 1975). Intergenerational transmission of psychopathology or abusive behavior may continue the cycle (Buist 1998). Given the incidence of postpartum disorders and the related behavioral and health concerns, relatively little clinical and research attention has been focused on understanding the causes and treatment of postpartum psychiatric disturbances. Progress may be hampered by the ethical and legal issues related to research involving a human fetus or infant (Shear and Mammen 1995). In addition, it is likely that research on postpartum disorders has failed to yield simple relationships that can be translated into clinical diagnosis and treatment, because such disorders are the result of complex associations of many variables. Extensive changes in hormones, fluids and electrolytes, neurotransmitters, and circadian rhythms occur during pregnancy and the puerperium and are often coupled with changes in the woman’s role, body image, marital relationship, and financial considerations (Boyce 1994; Shear and Mammen, 1995). Various personality and psychosocial measures (e.g., negative life events, parity, social support, and past history), as well as physiologic measures (e.g., cortisol, corticotropin-releasing hormone, thyroid hormones), have been related to human pre- and postpartum psychiatric disorders (Boyce 1994; Forman et al 2000; Handley et al 1980; Harris 1999; Harris et al 1992, 1996; Kendell et al 1987; Martin et al 1989; Pedersen et al 1993; Schmeelk et al 1999); however, not all studies find the same social, psychological, or biological factors to be related unequivocally to postpartum depression, which may be due to inconsistencies in the type and timing of measurement and the lack of consideration of multiple, diverse factors (O’Hara 1997). A nonhuman primate model offers many advantages for the study of complex processes with interrelated biological and psychological components. Control of environmental variables such as diet or substance abuse, direct measurement of behavior, documented early rearing history, and ability to manipulate the variables of interest are some of these advantages. Nonhuman primates often exhibit diseases and behaviors more similar to humans than do nonprimates, owing to their close phylogenetic relationship (Reite 1977). The relatively long gestation and period of infant dependency are also similarities between pri-

L. Brent et al

mates and humans not shared with many other mammals. Parenting in primates may also be more sensitive to experiential, cognitive, and social variables than in other mammals (Maestripieri 1999a; Pryce 1995). Nonhuman primates in captivity develop a wide array of pathologic and stereotypical behavior patterns, termed here as abnormal behaviors. Many abnormal behaviors in nonhuman primates are strikingly similar in form and occurrence to human behavioral pathologies (Berkson 1967; Berkson and Mason 1963). Rocking, hair plucking, stereotyped movements, and self-stimulatory behaviors are examples of primate abnormal behavior; and although all nonhuman primate abnormal behavior patterns may not correspond perfectly to human psychopathologies, their occurrence reflects compromised functioning and is often a response to stress. Measuring changes in the rates of such behaviors offers a method to study individual variation and gauge responsiveness to eliciting stimuli. Whereas characterization of human postpartum disorders usually uses questionnaires, measurements of behavioral or physiologic variables are usually done directly in animal models. The observed behavior of nonhuman primates is more a reflection of their internal state, without the complex filters of self-perception and ethics found in humans. A mother nonhuman primate that has an impulse to harm herself or her infant probably does so. Goosen (1981) noted that monkeys display in their behavior similar deviations that psychiatrists infer from their verbal interviews with human patients. For example, symptoms of human affective disorders include self-directed, negative communication analogous to the abnormal, selfdirected behaviors in the nonhuman primate. Nonhuman primate abnormal behavior may be related to inappropriate early rearing environments, extended periods of time without social contact, or inadequate space (Capitanio 1986), although severe abnormal behaviors can occur in socially reared monkeys (Erwin et al 1973). The prevalence of abnormal behavior is not consistent across individuals with similar rearing and housing histories, and a great deal of individual variation exists in the frequency and form of the behavior (Suomi 1982). Self-directed behavior has also been used as an indicator of stress and anxiety in primates, including baboons (Castles and Whiten 1998; Diezinger and Anderson 1986; Easley et al 1987; Maestripieri et al 1992). Scratching is more common during periods of stress, frustration, or anxiety, such as during crowding, cognitive challenge, aggression, and when neighbors vocalize (Aureli and de Waal 1997; Baker and Aureli 1997; Castles and Whiten 1998; Leavens et al 2001). Self-scratching has been evaluated as an indicator of anxiety in macaque mothers, with rates higher during the birth season than during the mating season and also higher during potentially danger-

Postpartum Behavior in Baboons

ous situations (Maestripieri 1993, 2000). In humans, measuring self-directed behavior can be useful in the diagnosis of psychiatric conditions (Fairbanks et al 1982; Troisi et al 2000). Abusive maternal behavior has also been observed in nonhuman primates (e.g., Reite and Caine 1983). The research of Maestripieri and colleagues in particular has increased our understanding of infant abuse in nonhuman primates. In a sample of eight pigtail macaques who displayed abusive behavior toward their infants, abuse began during the first week postpartum, the behaviors typically occurred after stressful situations, and abusive mothers generally possessed otherwise adequate mothering skills and social behavior compared with control animals who were not abusive (Maestripieri and Carroll 1998a). Such behaviors are usually consistent across subsequent births, distinct from neglect (which occurs more often in inexperienced mothers), and may be transmitted between generations (Maestripieri et al 1997, 1999). Abusive behaviors toward offspring probably represent a pathologic phenomenon rather than an adaptive form of reduced parental expenditure (Maestripieri 1998). Inadequate mothering has also been associated with previous depressive reactions to repeated separation from peers, indicating that monkeys experiencing depression are at risk for problems after the birth of the infant (Suomi and Ripp 1983). Most research on maternal stress and infant abuse among nonhuman primates has used small sample sizes, making generalizations difficult. In addition, no previous study has examined the incidence of abnormal behaviors across pregnancy and the puerperium. The purpose of this project was to determine the prevalence of behaviors related to stress and abnormal functioning over the course of pregnancy and the postpartum period in a relatively large sample of captive baboons. Abnormal behaviors and self-scratching were evaluated in the third trimester of pregnancy and over an 8-week period after birth. Because of the possible relation to stress and the negative effects on the infant, infant abuse was also measured in the postpartum period. The levels of abuse, abnormal behavior, and scratching were related to the mother’s age, parity, and dominance rank. We expected that the psychological and physiologic changes that occur postpartum may influence the stress that the mother experiences, resulting in measurable behavioral changes.

Methods and Materials Subjects and Housing The subjects of the study were 62 female olive baboons (Papio hamadryas anubis sp.) living in single-male social groups with approximately 30 other adult female baboons and their offspring.

BIOL PSYCHIATRY 2002;52:1047–1056

1049

Five mothers were primiparous, and the other 57 females had given birth to between 1 and 9 infants (mean ⫽ 3.6 infants, SD ⫽ 1.0) before the study began. No evidence of medical difficulties related to the birth of the infant (e.g., birth complications, infection) was noted in this subject pool. Subjects were between the ages of 5.7 and 19 years (mean ⫽ 12.6 years, SD ⫽ 3.2). All females had been raised by their mothers in similar social groups and cages. The baboons all lived in identical 500-square-foot outdoor enclosures, with climbing structures and heated indoor dens. All baboons were fed a commercially available diet once per day and provided with mixed grain at least once per week. The cages were cleaned each morning.

Data Collection and Analysis Pregnancy was determined by examining weekly records of the females’ estrus swelling pattern (see Strum and Western 1982), and an estimated date of parturition was assigned as 185 days past the date of conception. The actual date of parturition for females in this project averaged 5.3 days from the estimated date. During the third trimester of pregnancy, 10 30-min focal observations were collected using pen and paper, including records of the frequency of social behaviors, stress-related behaviors, and abnormal behaviors. To assess dominance level within our groups, we analyzed the frequency of aggressive, affiliative, and submissive behaviors between each subject and other group members during this prepartum data collection. In addition, we recorded the order that individuals within the group obtained fruit that was provided at the front of the cage. Dominance rank is usually related to the directionality of approach–retreat interactions or control of resources (Boelkins 1967; Walters and Seyfarth 1987). This measure of priority of access to a preferred food source, along with the frequency of social behaviors given and received, was used to group females into high (n ⫽ 12), medium (n ⫽ 32), and low (n ⫽ 18) dominance rank groups. Wild baboon females inherit their dominance status from their mothers and live in a matrilineal, or female-bonded, society. In this colony, subjects were generally unrelated to other group members in the cage. Dominance status was thus not socially transmitted from mother to daughter, but rather based on individual characteristics. Beginning on the day of birth and continuing for 8 weeks, 15-min focal observations were completed on each subject using a laptop computer and the Observer data collection program (Observer, Noldus Information Technology, Wageningen, Netherlands). During week 1, 20 observations were completed, 8 observations were completed in each of weeks 2– 4, and 4 observations were completed in each of weeks 5– 8. A total of 60 observations, or 15 hours, were collected for each subject unless she was hospitalized or the infant was removed from her due to poor maternal care, injury, or illness. A total of 249 hours of behavioral observations were completed in the prepartum period, and 884.5 hours were completed in the postpartum period. The data collection protocol allowed characterization of both common and infrequent behavior patterns. All observations were balanced for time of day. Observers with education and experience in behavioral primatology were thoroughly trained to collect behavioral data over a

1050

L. Brent et al

BIOL PSYCHIATRY 2002;52:1047–1056

Table 1. Definitions of Behaviors Recorded Behaviors Abusive Bite infant Dangle infant Drag infant Hit infant Let infant fall Pull infant’s hair Push infant Rough handling Ingestion-related abnormal behaviors Coprophagy Drink urine Feces painting Pull/eat hair

Definition Closing the teeth on infant’s body with enough pressure to cause injury Holding infant away from body and dangle infant by hands or feet above her body or out from her body; infant is distressed. Pulling infant across substrate by arm, leg, or tail Contacting infant forcefully with hand, slapping Not responding or repositioning infant when it begins to fall, resulting in the infant falling; infant is distressed. Yanking hair of infant aggressively Shoving infant forcefully away or mashing infant onto floor Aggressive or careless manipulation of infant, such as shaking

Ingesting feces Ingestion of own or other animal’s urine Smearing feces on cage, may lick feces or manipulate orally Plucking or yanking out hair of self or other and ingesting the hair; may pick hair off floor and eat it Regurgitation Coughing up already-swallowed food, usually into cheek pouches, and reingesting vomitus; may be accompanied by leaning forward Repetitive and stereotypical abnormal behaviors Head toss Throwing head back and moving it to the side in a circular manner Pace Walking in the same pattern, recorded when observed for more than one repetition Rock Back-and-forth or side-to-side movement, can be sitting or standing, but involves entire upper body Stereotyped movement Whole-body movements other than pacing or rocking Self-directed abnormal behaviors Bizarre posture Holding seemingly uncomfortable or unnatural posture, often by holding the leg behind the head Eye poke Pushing digit into eye, may hold hand in saluting position against head Floating limb Limb raises into air, subject may watch limb as if the subject is not in control of it Self-aggression Violence directed toward one’s own body, such as biting, hitting, and slamming self against cage of a severity to cause pain or injury Suck self Sucking part of body for an extended period of time Stress-related Scratch self Use of finger, hand, or foot to rake across the skin

4 – 6-month training period. Interobserver reliability testing was conducted during this time period, and observers were not considered reliable until 85% or better agreement with the first author was consistently obtained. In addition, to insure that the two different data collection methods did not bias the results of the study, reliability testing was conducted between an observer recording the mother’s behavior on paper and one using the computer. Average interobserver reliability scores for scratching were over 93%, and those for abnormal behavior were 85%. The behaviors we analyzed for the study included abnormal behaviors, infant abuse, and self-scratching as a measure of stress (see Table 1). Abusive behaviors were directed specifically at the infant, usually resulted in stress behaviors and vocalizations from the infant, and may have caused harm to the infant. Abnormal behaviors were categorized by type: ingestion-related behaviors, repetitive and stereotypical behaviors, and self-directed behaviors. Data were summarized for each subject for each behavior category as the mean prepartum and postpartum frequency per hour. In addition, postpartum data were further divided by week to measure changes over time.

The prevalence of abnormal, abusive, and stress-related behaviors in the population was calculated as the proportion of females displaying the behavior at least once in the pre- and postpartum period. Paired comparison t tests were used to compare the mean frequency per hour of occurrence in each behavior category in the prepartum period with the postpartum period. Pearson correlations, with Bonferroni adjustment for multiple comparisons, were used to determine the relationships between 1) different behavior categories; 2) prepartum and postpartum levels of abnormal behavior and scratching; and 3) the females’ age and number of offspring and each behavior category. Repeated measures analysis of variance procedures, with rank group as a categorical factor, were used to evaluate any changes over time (week) and any influence of the mothers’ dominance level. Most of the statistical tests included all 62 baboon subjects. Because 11 females had missing observations for certain weeks during the postpartum time frame due to illness or injury of the mother or infant, only the 51 subjects with complete data were

Postpartum Behavior in Baboons

Figure 1. The proportion of different abusive behaviors toward the infant.

used in the analysis of changes over time. In addition, abnormal behaviors of some subjects were not consistently recorded early in the study, so that comparisons of prepartum with postpartum frequencies of abnormal measures included 44 animals. Significance was two-tailed, defined as p ⬍ .05, and potential trends are designated as p ⬍ .10.

BIOL PSYCHIATRY 2002;52:1047–1056

1051

tum period. The total frequency of abnormal behavior was 0.68 times per hour per subject prepartum, which rose to 2.36 incidences per hour postpartum, a highly significant increase [t(43) ⫽ 2.70, p ⬍ .009]. The number of females displaying all three types of abnormal behaviors rose in the postpartum period (ingestion: pre 43.2% vs. post 96.8%; repetitive: pre 18.2% vs. post 24.2%; self-directed: pre 2.3% vs. post 33.9%). The frequency of ingestion-related behaviors [t(43) ⫽ 2.97, p ⬍ .005] and self-directed behaviors [t(43) ⫽ 2.73, p ⬍ .009] were significantly higher in the postpartum period, whereas repetitive behaviors showed a trend toward significance [t(43) ⫽ 1.73, p ⬍ .091]. Figure 2 illustrates the frequency of these behaviors. Of particular interest is the behavior of one female, who developed a series of repetitive, idiosyncratic behaviors after she gave birth. She would slowly walk her feet up the wall of the enclosure until she was standing on her hands with the infant clinging to her belly, and then slap the floor with her hands rhythmically for several seconds. The cycle was repeated dozens of times during the postpartum period, although it was not exhibited prepartum. We have never seen this behavior in any other baboon in our colony. Self-scratching is a common behavior and occurred in 72.6% of females in the prepartum period and all females in the postpartum. The frequency of scratching rose significantly during the postpartum period [t(61) ⫽ 14.86, p ⬍ .001] from a mean of 4.9 times per hour prepartum to 22.0 times per hour postpartum.

Results Prevalence of Abusive, Abnormal, and StressRelated Behaviors during the Prepartum and Postpartum Periods The prevalence of abusive behaviors was fairly high in the postpartum period. Of the 62 subjects, 34 mothers exhibited 159 abusive behaviors, but half of occurrences (50.1%) were attributable to only four subjects. The four subjects ranged in age from 9.4 to 15.1 years, had between two and five previous infants, and three were low ranking and one was medium ranking. Three of the females successfully raised two or more infants before the current one, and one baboon had two previous infants that died within days of birth. During the first week postpartum, maternal abuse resulted in the death of one infant and the removal of another infant from the mother for medical treatment. The incidence of different types of abusive behavior is displayed in Figure 1. Abnormal behaviors occurred in 52.3% of the subjects during the prepartum period, and all but one subject (98.4%) displayed abnormal behavior during the postpar-

Figure 2. All three categories of abnormal behavior increased in the postpartum period.

1052

BIOL PSYCHIATRY 2002;52:1047–1056

Figure 3. Self-scratching and ingestion-related behaviors increased significantly over the 8-week postpartum period. Lowranking females had higher levels of abusive behavior during weeks 2 and 7.

Females who had exhibited abnormal behavior in the prepartum period were more likely to have abnormal behavior in the postpartum (r ⫽ 0.71, p ⬍ .001). Levels of self-scratching were not correlated between the pre- and postpartum periods.

Changes in Behaviors over Time and Relationship with Other Variables No significant correlations were found between the frequencies of the three abnormal behaviors, self-scratching, and total abusive behavior or with the mother’s age or the number of previous births; however, several behaviors changed significantly over the 8-week postpartum period. Ingestion-related behaviors [F(7336) ⫽ 2.10, p ⬍ .043] and self-scratching [F(7336) ⫽ 20.15, p ⬍ .001] increased over time. Figure 3 displays the changes in these behaviors over the 8-week data collection period. The only behavior category that was related to the mother’s background was the frequency of abuse. The mean frequency per hour of abusive behavior was highest for low-ranking females (low rank: ⫽ 0.67, SD ⫽ 0.9; medium rank: ⫽ 0.20, SD ⫽ 0.6; high rank: ⫽ 0.10, SD ⫽ 0.2). An interaction between dominance rank and week was significant [F(14,336) ⫽ 2.11, p ⬍ .011], with low-ranking females displaying peaks in abusive behaviors during weeks 2 and 7 postpartum (see Figure 3).

Discussion This project investigated pathologic and stress-related behaviors across pregnancy and the postpartum period in a

L. Brent et al

nonhuman primate. The prevalence and frequency of abnormal behaviors were significantly higher in the postpartum period than during pregnancy in a captive population of baboons. Self-scratching, a common behavior indicative of perceived stress, frustration or anxiety in primates, also increased significantly after the birth of the baboon mother’s infant. Thus, the levels of abnormal behavior patterns and scratching indicate that female baboons exhibit signs of stress and behavioral pathology at an increased rate during the postpartum period as compared with the prepartum period, providing evidence that motherhood and the presence of infants can entail heightened levels of anxiety (Maestripieri 1993). These indices may provide useful measures to study postpartum disorders in a nonhuman primate model. Symptoms of depression, anxiety, or other disturbances during pregnancy in humans have been consistently related to postpartum depressive symptoms and psychoses and can be considered risk factors for psychiatric disturbances after the birth of the infant (e.g., Kendell et al 1987; O’Hara et al 1991; Watson et al 1984). The level of abnormal behavior in baboons during pregnancy was highly correlated with abnormal levels in the postpartum. As in humans, there appears to be continuity among individuals with increased vulnerability to distress during pregnancy and after birth. The frequency of self-scratching and abnormal behaviors related to ingestion increased over the first 2 months postpartum. Baboon maternal stress and anxiety, as measured by abnormal behavior and scratching frequency, is probably not a transient occurrence related to the novelty of the new infant, but more likely a reflection of the social and physiologic changes related to motherhood. A relationship between the levels of scratching and abnormal or abusive behavior was not found, but this may reflect differential adjustments to a similar stressor among individuals. It is clear from our study that a change in self-directed and abnormal behavior occurred after the birth of the subjects’ infants; however, it is possible that this finding could result either from an increase in such behaviors postpartum or a depression in these behaviors during the prepartum period. Unfortunately, baseline data from the same subjects during nonpregnant periods without offspring is unavailable to answer this question, because in this breeding colony, mothers are typically pregnant again before their older offspring is weaned. A comparison with other data provides guidance. A survey of abnormal behavior conducted previously in the same colony indicated that 51% of 100 female subjects displayed at least one type of abnormal behavior (Brent, unpublished data). The prevalence rate in this survey is similar to our data during the prepartum period (52%) and much lower than during the postpartum period (98%). The

Postpartum Behavior in Baboons

frequency of scratching during the postpartum period for our subjects was higher than that reported for captive male baboons (Easley et al 1987) or macaques (Diezinger and Anderson 1986; Maestripieri 2000) but similar to rates reported for wild male and female baboons after an aggressive interaction (Castles and Whiten 1998). Based on these comparisons, the most likely explanation for the change in behavior in our study is that the females experienced an increase in stress-related scratching and abnormal behaviors during the postpartum. Although comparative information does not exist for the rate of abnormal and scratching behavior in nonhuman primates during pregnancy and after parturition, abusive behaviors have been studied (see Maestripieri and Carroll 1998b). Surveys of abuse in several nonhuman primate species indicate that the incidence and severity of abuse varies across primate species, with 10% to over 30% of youngsters experiencing abuse (Caine and Reite 1983; Schapiro and Mitchell 1983), although in these studies the actual perpetrator of abuse was unknown. In a more recent review of colony records of infant pigtail macaques over a 33-year time span, 37 cases of maternal abuse resulted in the death or removal of the infant from the mother for medical treatment (Maestripieri et al 1997). This severe level of abuse occurred in 17 of a total of 71 mothers, and maternal abuse was more likely to occur in closely related females within only three of five groups, offering evidence that abusive behaviors are passed between generations through observation or other mechanisms (Maestripieri et al 1997). A survey of the incidence of human physical child abuse in two-parent households is very similar to our data on baboon maternal abuse. Gelles and Straus (1979) reported that 63% of parents used at least one form of violence toward their children, including spanking or slapping (58%), hitting with an object (13%), throwing an object at the child (5%), and kicking, biting, or hitting with the fist (3%). Overall, 3.6% of the parents used a method of abuse severe enough to injure the child (Gelles and Straus 1979). In our study with 62 mothers, over 50% exhibited at least one instance of abuse, but death or removal of the infant for injury occurred in only 3.2% of mothers during the first 8 weeks postpartum. The course of abuse in this study differed from that reported in macaque species, in which abusive mothers generally had the highest levels of abuse during week 1, which decreased over 12 weeks (Maestripieri 1998; Maestripieri and Carroll 1998a; Maestripieri et al 1999). In this study, abuse showed no evidence of a decline over the 8-week period; however, Maestripieri and colleagues’ estimation of abuse rates used smaller samples, consisting only of females known to be abusive (Maestripieri 1998; Maestripieri and Carroll 1998a; Maestripieri et al 1999). If

BIOL PSYCHIATRY 2002;52:1047–1056

1053

we include only the most abusive baboon mothers (with a mean abuse frequency greater than or equal to 0.5 times per hour), we find that the rate of abuse is similar to the macaque study with the exception that levels do not decrease over time. The temporal changes in infant abuse may differ between species, or the larger sample size used here may provide a different picture of abusive tendencies. Abusive behavior was not related to the mother’s parity or age, but was related to maternal dominance rank. Studies of abusive behavior in humans and socially raised, nonhuman primates indicates that abuse is not related to birth order (Field 1983; Maestripieri 1999b; Schapiro and Mitchell 1983). Although dominance rank has not been previously analyzed in relation to infant abuse, this study’s finding that subjects with low dominance rank had higher levels of abusive behavior may be a reflection of the individual’s increased social stress and decreased ability to interact positively with others. Abusive behavior may be an inappropriate attempt to control the infant’s behavior as a maladaptive response to stress (Maestripieri 1998). Individuals with lower dominance often have limited social support, experience more harassment or kidnapping of their infant, and have less access to preferred foods (Altmann 1980; Maestripieri 1994; Silk 1987). Lowranking nonhuman primate mothers are known to be more protective of their infants (Altmann 1980) and to avoid high-ranking individuals (Maestripieri 1995). Because other baboons are highly interested in infants (Altmann 1980), it is not surprising that individuals with low dominance levels experience a particularly difficult adjustment to the increased attention and demands of motherhood. A parallel may be drawn between the finding in baboons and humans, as a lack of social support and a poor relationship with the spouse have consistently been linked to postpartum depression (Campbell et al 1992; O’Hara et al 1983; Paykel et al 1980) and child abuse (Smith and Hanson 1975). A benefit of the current study is that it involved normally occurring variation in pathologic and stressrelated behaviors in a large population of socially reared baboons, rather than an animal model in which psychological disorders were induced by separation from the mother and/or social and physical isolation (e.g., Benhar 1977; McKinney 1984; Reite 1977) or through pharmacologic intervention (e.g., Friedman et al 1988; Palit et al 1998). Thus, the level of abnormal behavior may reflect the individual’s temperament and response to stress, the influence of their mother’s style, or underlying genetic predisposition. The current study supports the concept of postpartum pathologic behaviors existing as a continuous distribution of behaviors rather than as a discrete category (see Antony et al 1998; Kendler and Gardner 1998; Weinberg et al

1054

BIOL PSYCHIATRY 2002;52:1047–1056

2001). Abnormal behaviors were found in many mothers at low levels during pregnancy and increased in frequency after the birth of the infant. Abusive behaviors were fairly common but varied quantitatively among subjects. Although it may not be possible to categorize the pathologic behavior of nonhuman primates into discrete syndromes, the prevalence and occurrence of such behaviors can be used to gauge changes over different environmental conditions as well as to relate them to genetic, behavioral, and physiologic influences. This study indicates that the baboon may be a useful model for the study of postpartum disorders.

This project was supported by National Institutes of Health Grants MH58732 and RR13199. The authors thank Michelle Foley and Stacey Evans, who helped collect the data, and Linda Freeman Shade, who wrote computer subroutines to analyze the data. We also thank three anonymous reviewers for their helpful comments on the manuscript. The Southwest Foundation for Biomedical Research and Southwest National Primate Research Center are fully accredited by the Association for Accreditation of Laboratory Animal Care International and follow all applicable regulations. All procedures used in this study were approved by the Institutional Animal Care and Use Committee.

References Adshead G, Brooke D, Samuels M, Jenner S, Southall D (2000): Maternal behaviors associated with smothering: A preliminary descriptive study. Child Abuse Negl 24:1175–1183. Altmann J (1980): Baboon Mothers and Infants. Cambridge: Harvard University Press. Altshuler LL, Hendrick V, Cohen LS (1998): Course of mood and anxiety disorders during pregnancy and the postpartum period. J Clin Psychiatry 59:29 –33. Antony MM, Downie F, Swinson RP (1998): Diagnostic issues and epidemiology in obsessive-compulsive disorder. In: Swinson RP, Antony MM, Rachman S, Richter MA, editors. Obsessive-Compulsive Disorder: Theory, Research, and Treatment. New York: The Guilford Press, pp 3–32. Aureli F, de Waal FBM (1997): Inhibition of social behavior in chimpanzees under high-density conditions. Am J Primatol 41:213–228. Baker KC, Aureli F (1997): Behavioural indicators of anxiety: An empirical test in chimpanzees. Behaviour 134:1031–1050. Benhar E (1977): The olive baboon (Papio anubis) as an animal model for research in affective disorders of man. Lab Anim Sci 27:887–894. Berkson G (1967): Abnormal stereotyped motor acts. In: Zubin J, Hunt HF, editors. Comparative Psychopathology, Animal and Human. New York: Grune & Stratton, pp 76 –94. Berkson G, Mason WA (1963): Stereotyped movements of mental defectives: III. Situation effects. Am J Ment Defic 68:409 –412. Boelkins RC (1967): Determination of dominance hierarchies in monkeys. Psychonom Sci 7:317–318.

L. Brent et al

Boyce P (1994): Personality dysfunction, marital problems and postnatal depression. In: Cox J, Holden J, editors. Perinatal Psychiatry: Use and Misuse of the Edinburgh Postnatal Depression Scales. London: Gaskell, pp 82–102. Brockington I (1996): Motherhood and Mental Health. Oxford: Oxford University Press. Brockington IF, Cernik KF, Schofield EM, Downing AR, Francis AF, Keelan C (1981): Puerperal psychosis. Phenomena and diagnosis. Arch Gen Psychiatry 38:829 –833. Buist A (1998): Childhood abuse, postpartum depression and parenting difficulties: A literature review of associations. Aust N Z J Psychiatry 32:370 –378. Caine N, Reite M (1983): Infant abuse in captive pig-tailed macaques: Relevance to human child abuse. In: Reite M, Caine NG, editors. Monographs in Primatology: Volume 1. Child Abuse: The Nonhuman Data. New York: Alan R. Liss, pp 19 –27. Campbell SB, Cohn JF, Flanagan C, Popper S, Meyers T (1992): Course and correlates of postpartum depression during the transition to parenthood. Dev Psychopathol 4:29 –47. Capitanio JP (1986): Behavioral pathology. In: Mitchell G, Erwin J, editors. Comparative Primate Biology, Volume 2A. Behavior, Conservation, and Ecology. New York: Alan R. Liss, pp 411–454. Castles DL, Whiten A (1998): Post-conflict behaviour of wild olive baboons. II. Stress and self-directed behaviour. Ethology 104:148 –160. Cooper PJ, Murray L (1995): Course and recurrence of postnatal depression: Evidence for the specificity of the diagnostic concept. Br J Psychiatry 166:191–195. Diezinger F, Anderson JR (1986): Starting from scratch: A first look at a “displacement activity” in group-living rhesus monkeys. Am J Primatol 11:117–124. Easley SP, Coelho AM Jr, Taylor LL (1987): Scratching, dominance, tension, and displacement in male baboons. Am J Primatol 13:397–411. Erwin J, Mitchell G, Maple T (1973): Abnormal behavior in non-isolate-reared rhesus monkeys. Psychol Rep 33:515–523. Fairbanks LA, McGuire MT, Harris CJ (1982): Nonverbal interaction of patients and therapists during psychiatric interviews. J Abnorm Psychol 91:109 –119. Field T (1983): Child abuse in monkeys and humans: A comparative perspective. In: Reite M, Caine NG, editors. Monographs in Primatology: Volume 1. Child Abuse: The Nonhuman Primate Data. New York: Alan R. Liss, pp 151–174. Forman DN, Videbech P, Hedegaard M, Salvig JD, Secher NJ (2000): Postpartum depression: Identification of women at risk. Br J Obstet Gynaecol 107:1210 –1217. Friedman S, Sunderland GS, Rosenblum LA (1988): A nonhuman primate model of panic disorder. Psychiatry Res 23:65– 75. Galler JR, Harrison RH, Ramsey F, Forde V, Butler SC (2000): Maternal depressive symptoms affect infant cognitive development in Barbados. J Child Psychol Psychiatry Allied Discip 41:747–757. Gelles RJ, Straus MA (1979): Violence in the American family. J Soc Issues 35:5–39.

Postpartum Behavior in Baboons

BIOL PSYCHIATRY 2002;52:1047–1056

1055

Goosen C (1981): Abnormal behavior patterns in rhesus monkeys: Symptoms of mental disease? Biol Psychiatry 16:697– 716.

Maestripieri D (2000): Measuring temperament in rhesus macaques: Consistency and change in emotionality over time. Behav Processes 49:167–171.

Handley SL, Dunn TL, Waldron G, Baker JM (1980): Tryptophan, cortisol and puerperal mood. Br J Psychiatry 136:498 – 508.

Maestripieri D, Carroll KA (1998a): Behavioral and environmental correlates of infant abuse in group-living pigtail macaques. Infant Behav Dev 21:603–612.

Harris B (1999): Postpartum depression and thyroid antibody status. Thyroid 9:699 –703.

Maestripieri D, Carroll KA (1998b): Child abuse and neglect: Usefulness of the animal data. Psychol Bull 123:211–223.

Harris B, Lovett L, Smith J, Read G, Walker R, Newcombe R (1996): Cardiff puerperal mood and hormone study. III. Postnatal depression at 5 to 6 weeks postpartum, and its hormonal correlates across the peripartum period. Br J Psychiatry 168:739 –744.

Maestripieri D, Schino G, Aureli F, Troisi A (1992): A modest proposal: Displacement activities as an indicator of emotions in primates. Anim Behav 44:967–979.

Harris B, Othman S, Davies JA, Weppner GJ, Richards CJ, Newcombe RG, et al (1992): Association between postpartum thyroid dysfunction and thyroid antibodies and depression. Br Med J 305:152–156. Hay DF (1997): Postpartum depression and cognitive development. In: Murray L, Cooper PJ, editors. Postpartum Depression and Child Development. New York: The Guilford Press, pp 85–110. Jennings KD, Ross S, Popper S, Elmore M (1999): Thoughts of harming infants in depressed and nondepressed mothers. J Affect Disord 54:21–28. Kendell RE, Chalmers JC, Platz C (1987): Epidemiology and puerperal psychoses. Br J Psychiatry 150:662–673. Kendler KS, Gardner CO Jr (1998): Boundaries of major depression: An evaluation of DSM-IV criteria. Am J Psychiatry 155:172–177. Kessler RC, McGonagle KA, Zhao S, Nelson CB, Hughes M, Eshleman S, et al (1994): Lifetime and 12-month prevalence of DSM-III-R psychiatric disorders in the United States: Results from the National Comorbidity Survey. Arch Gen Psychiatry 51:8 –19. Lanczik M, Hofberg K, Brockington IF (1999): Delusion of infestation with post-partum onset: Case report. Psychopathology 32:277–280. Leavens DA, Aureli F, Hopkins WD, Hyatt CW (2001): Effects of cognitive challenge on self-directed behaviors by chimpanzees (Pan troglodytes). Am J Primatol 55:1–14. Maestripieri D (1993): Maternal anxiety in rhesus macaques (Macaca mulatta). I. Measurement of anxiety and identification of anxiety-eliciting situations. Ethology 95:19 –31. Maestripieri D (1994): Infant abuse associated with psychosocial stress in a group-living pigtail macaque (Macaca nemestrina) mother. Am J Primatol 32:41–49. Maestripieri D (1995): Assessment of danger to themselves and their infants by rhesus macaque (Macaca mulatta) mothers. J Comp Psychol 109:416 –420. Maestripieri D (1998): Parenting styles of abusive mothers in group-living rhesus macaques. Anim Behav 55:1–11. Maestripieri D (1999a): Fatal attraction: Interest in infants and infant abuse in rhesus macaques. Am J Phys Anthropol 110:17–25. Maestripieri D (1999b): The biology of human parenting: Insights from nonhuman primates. Neurosci Biobehav Rev 23:411–422.

Maestripieri D, Tomaszycki M, Carroll KA (1999): Consistency and change in the behavior of rhesus macaque abusive mothers with successive infants. Dev Psychobiol 34:29 –35. Maestripieri D, Wallen K, Carroll KA (1997): Infant abuse runs in families of group-living pigtail macaques. Child Abuse Negl 21:465–471. Marks MN, Kumar R (1993): Infanticide in England and Wales. Med Sci Law 33:329 –339. Martin CJ, Brown GW, Goldberg DP, Brockington IF (1989): Psycho-social stress and puerperal depression. J Affect Disord 16:283–293. McKinney WT (1984): Animal models of depression: An overview. Psychiatr Dev 2:77–96. Murray L, Cooper PJ (1997): The role of infant and maternal factors in postpartum depression, mother-infant interactions, and infant outcome. In: Murray L, Cooper PJ, editors. Postpartum Depression and Child Development. New York: The Guilford Press, pp 111–135. O’Hara MW (1997): The nature of postpartum depressive disorders. In: Murray L, Cooper PJ, editors. Postpartum Depression and Child Development. New York: The Guilford Press, pp 3–31. O’Hara MW, Rehm LP, Campbell SB (1983): Postpartum depression: A role for social network and life stress variables. J Nerv Ment Dis 171:336 –341. O’Hara MW, Schlecte JA, Lewis DA, Varner MW (1991): Controlled prospective study of postpartum mood disorders: Psychological, environmental, hormonal variables. J Abnorm Psychol 100:63–73. O’Hara MW, Zekoski EM, Philipps LH, Wright EJ (1990): Controlled prospective study of postpartum mood disorders: Comparison of childbearing and nonchildbearing women. J Abnorm Psychol 99:3–15. Palit G, Kumar R, Chowdhury SR, Gupta MB, Saxena RC, Srimal RC, et al (1998): A primate model of anxiety. Eur Neuropsychopharmacol 8:195–201. Paykel ES, Emms EM, Fletcher J, Rassaby ES (1980): Life events and social support in puerperal depression. Br J Psychiatry 136:339 –346. Pedersen CA (1999): Postpartum mood and anxiety disorders: A guide for the nonpsychiatric clinician with an aside on thyroid associations with postpartum mood. Thyroid 9:691–697. Pedersen CA, Stern RA, Pate J, Senger MA, Bowes WA, Mason GA (1993): Thyroid and adrenal measures during late pregnancy and the puerperium in women who have been major depressed or who become dysphoric postpartum. J Affect Disord 29:201–211.

1056

BIOL PSYCHIATRY 2002;52:1047–1056

Pitt B (1973): Maternity blues. Br J Psychiatry 122:431–433. Prodgers A (1984): Psychopathology of the physically abusing parent: A comparison with the borderline syndrome. Child Abuse Negl 8:411–424. Pryce CR (1995): Determinants of motherhood in human and nonhuman primates. In: Pryce CR, Martin RD, Skuse D, editors. Motherhood in Human and Nonhuman Primates. Third Schultz-Biegert Symposium, Kartause, Ittingen, 1994. Basel: Karger, pp 1–15. Reite M (1977): Maternal separation in monkey infants: A model of depression. In: Hanin I, Usdin E, editors. Animal Models in Psychiatry and Neurology. New York: Pergamon Press, pp 127–139. Reite M, Caine NG, editors (1983): Child abuse: The nonhuman primate data. In: Altmann J, Clarkson TB, Erwin J, Goldsmith EI, Mitchell G, Moor-Jankowski J, Southwick C, series editors. Monographs in Primatology: Volume 1. Child Abuse: The Nonhuman Primate Data. New York: Alan R. Liss. Robling SA, Paykel ES, Dunn VJ, Abbott R, Katona C (2000): Long-term outcome of severe puerperal psychiatric illness: A 23 year follow-up study. Psychol Med 30:1263–1271. Rogers JA (1983): Child abuse in humans: A clinician’s view. In: Reite M, Caine NG, editors. Monographs in Primatology, Volume 1. Child Abuse: The Nonhuman Primate Data. New York: Alan R. Liss, pp 1–17. Saintfort R, Stern TA (2000): Cross-cultural and neuropsychiatric aspects of a postpartum delusional state. Harv Rev Psychiatry 8:141–147. Schapiro SJ, Mitchell G (1983): Infant-directed abuse in a seminatural environment: Precipitating factors. In: Reite M, Caine NG, editors. Monographs in Primatology, Volume 1. Child Abuse: The Nonhuman Primate Data. New York: Alan R. Liss, pp 29 –48. Schmeelk KH, Granger DA, Susman EJ, Chrousos GP (1999): Maternal depression and risk for postpartum complications: Role of prenatal corticotropin-releasing hormone and interleukin-1 receptor antagonist. Behav Med 25:88 –94. Shear MK, Mammen O (1995): Anxiety disorders in pregnant and postpartum women. Psychopharmacol Bull 31:693–703.

L. Brent et al

Sichel DA, Cohen LS, Dimmock JA, Rosenbaum JF (1993): Postpartum obsessive compulsive disorder: A case series. J Clin Psychiatry 54:156 –159. Silk JB (1987): Social behavior in evolutionary perspective. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RM, Struhsaker TT, editors. Primate Societies. Chicago: University of Chicago Press, pp 318 –329. Smith SM, Hanson R (1975): Interpersonal relationships and child-rearing practices in 214 parents of battered children. Br J Psychiatry 127:513–525. Stowe ZN, Nemeroff CB (1995): Women at risk for postpartumonset major depression. Am J Obstet Gynecol 173:639 –645. Strum SC, Western JD (1982): Variations in fecundity with age and environment in olive baboons (Papio anubis). Am J Primatol 3:61–76. Suomi SJ (1982): Abnormal behavior and primate models of psychopathology. In: Fobes JL, King JE, editors. Communication and Behavior. An Interdisciplinary Series: Primate Behavior. New York: Academic Press, pp 171–215. Suomi SJ, Ripp C (1983): A history of motherless mother monkey mothering at the University of Wisconsin Primate Laboratory. In: Reite M, Caine NG, editors. Monographs in Primatology, Volume 1. Child Abuse: The Nonhuman Primate Data. New York: Alan R. Liss, pp 49 –78. Troisi A, Belsanti S, Bucci AR, Mosco C, Sinti F, Verucci M (2000): Affect regulation in alexithymia: An ethological study of displacement behavior during psychiatric interviews. J Nerv Ment Dis 188:13–18. Walters JR, Seyfarth RM (1987): Conflict and cooperation. In: Smuts BB, Cheney DL, Seyfarth RM, Wrangham RW, Struhsaker TT, editors. Primate Societies. Chicago: The University of Chicago Press, pp 306 –317. Watson JP, Elliott SA, Rugg AJ, Brough DI (1984): Psychiatric disorder in pregnancy and the first postnatal year. Br J Psychiatry 144:453–462. Weinberg MK, Tronick EZ, Beeghly M, Olson KL, Kernan H, Riley JM (2001): Subsyndromal depressive symptoms and major depression in postpartum women. Am J Orthopsychiatry 71:87–97.