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. Author manuscript; available in PMC: 2019 Nov 11.
Published in final edited form as: J Med Primatol. 2018 May 11:10.1111/jmp.12350. doi: 10.1111/jmp.12350

Maternal activity, anxiety, and protectiveness during moderate nutrient restriction in captive baboons (Papio sp.)

Lydia E O Light 1,2, Thad Q Bartlett 2, Annica Poyas 2, Mark J Nijland 3, Hillary F Huber 4, Cun Li 4, Kate Keenan 5, Peter W Nathanielsz 4,6
PMCID: PMC6230519  NIHMSID: NIHMS960095  PMID: 29749628

Abstract

Background

We hypothesized that maternal nutrient restriction (NR) would increase activity and behavioral indicators of anxiety (self-directed behaviors, SDB) in captive baboons (Papio sp.), and result in more protective maternal styles.

Methods

Our study included 19 adult female baboons. Seven females ate ad libitum (control group) and eight females ate 30% less (NR group) and were observed through pregnancy and lactation.

Results

Control females engage in higher rates of SDB than NR females overall (p ≤ 0.018) and during the prenatal period (p ≤ 0.001) and engage in more aggressive behavior (p ≤ 0.033). Control females retrieved infants more than NR females during weeks 5-8 postpartum (p ≤ 0.019).

Conclusions

Lower SDB rates among prenatal NR females reduce energy expenditure and increase available resources for fetal development when nutritionally restricted. Higher infant retrieval rates by controls may indicate more infant independence rather than maternal style differences.

Keywords: developmental programming, nutrition, mother-infant interactions

Introduction

Poor nutrition during pregnancy has significant negative effects on fetal growth, offspring health, and subsequent cognitive, behavioral, and emotional function in humans and several animal species [1–8]. While low birth weight is one outcome observable at birth, poor maternal nutrition has also been found to increase the risk for adult-onset conditions, including hypertension, cardiovascular disease, obesity, and diabetes [1]. In addition to physiological changes, prenatal undernutrition has been shown to alter cognitive performance of the offspring in a variety of species. For example, in sheep, Erhard et al. [9] found that ewes fed 50% less than control ewes during the first two-thirds of gestation had offspring with increased emotional reactivity and male offspring showed reduced cognitive flexibility, having difficulty transferring learning between tasks. Both male and female sheep also displayed sex-specific changes in side preferences during a T-maze test with males shifting from a right-bias to neutral and females shifting to a left-bias. In baboons, juvenile offspring of nutrient restricted mothers demonstrated less motivation and impaired working memory and male offspring of these same mothers showed impaired learning and increased impulsivity [8]. Similar deficits in cognitive flexibility and increased emotional reactivity have been found in other animal models [10]. Interestingly, cognitive inflexibility has been found in both prenatal and grand-maternal malnutrition in rats [11], suggesting developmental malnutrition may lead to permanent and heritable changes in cognition.

The field of developmental programming suggests that these enduring outcomes are the result of specific insults during critical periods in the development of the organism [3, 5, 12–15]. The mechanisms by which these behavioral changes occur remain elusive. A number of nonexclusive biological mechanisms have been proposed, including changes in organ structure, changes in organ cell number, clonal selection, metabolic differentiation (including changes to hormone and enzyme activity and epigenetic gene regulation), and the polyploidization of the main cells of the liver [2, 14, 15]. The role of hormones as the programming mechanism, particularly those involved with regulation of the hypothalamic-pituitary-adrenal (HPA) axis, has received considerable attention from researchers examining nutrient restriction (NR) in rodents and sheep [16–19].

Our research on the long-term effects of moderate global maternal nutrient restriction during pregnancy and lactation in socially-housed baboons (Papio sp.) looks at the effects of nutrient restriction across a variety of physiological processes [8, 20–34]. The results from these studies have confirmed that offspring born to mothers restricted to 70% of normal nutrient intake weigh approximately 12% less than offspring born to unrestricted mothers and said offspring have thus been described as intrauterine growth restricted (IUGR) [35]. The IUGR individuals included in our studies demonstrate a number of physiological, cognitive, and behavioral differences when compared to individuals who developed under nutritional control conditions. For example, IUGR resulted in upregulation of the HPA axis [26], increased fetal cortisol [34], impaired ventricular function [33], insulin resistance [21], premature brain aging among females [32], reduced cognitive flexibility [8], and behavioral changes including low arousal, poor attention, and a difficulty modulating activity [36]. Furthermore, IUGR offspring displayed increased aggression at 3-5 years of age, particularly among males [23]. In that study, Huber and colleagues speculated that one unexplored explanation for the increased aggression may have been social, with aggression being a behavior learned from their NR mothers, as maternal behavior in nonhuman primates has been shown to have considerable effects on adult offspring behavior [37, 38]. However, little is currently known about how changes in maternal behavior and performance contribute to long term behavioral/cognitive outcomes in offspring of nutrient restricted mothers [17, 39]. Therefore, in the current study, we explore maternal behavior and performance during NR to better understand the variety of mechanisms that may be influencing these negative outcomes.

A number of studies have demonstrated that maternal behavior, especially that pertaining to anxiety and mother-infant interactions, can have long-lasting effects on offspring behavior during adulthood among nonhuman primates [40–44] and other animals [9, 17, 45, 46]. In particular, maternal style has been determined to play a central role in the development of individual temperament [47–50], including patterns of reactions to stress [40, 41, 51, 52] and future maternal behavior [42].

In this study we investigated self-directed behavior (SDB), an often used indicator of anxiety in nonhuman primates [41, 53–55], and social interactions in NR mothers both before and after parturition, as well as a number of aspects of mother-infant interactions during infancy. Research on NR has generated (albeit mostly anecdotal) reports of adverse effects on sociability and temperament in nonhuman primates [56], increases in activity levels and stereotypic behaviors in nonhuman primates [57], and increased levels of glucocorticoids in rodents [18, 19, 58]. Our team has now demonstrated that NR in baboons can result in increased fetal cortisol levels and an up-regulation of the HPA axis in fetal baboons [26, 59]. We therefore hypothesized that NR females would show increased activity levels, reduced sociability, increased rates of aggression, and increased rates of SDB compared to control females. Also, because the presence of an infant following birth increases overall rates of sociality [60] and SDB rates have been shown to increase after birth [41], we expected that rates of aggression and SDB would be greatest in NR mothers during the postpartum period.

If NR results in an increase in stress, maternal style also may be affected. Female baboons of low rank are known to be more protective of their infants [42, 61–64] and it has been suggested that this is the result of increased stress due to limited social support networks [41]. Furthermore, baboon females typically experience an increase in cortisol during the last two weeks of gestation that has been correlated with increased mother-infant affiliative interactions after parturition [65] and mothers who are more attentive to infant distress signals during the first eight weeks of life [66]. It thus follows that anxiety due to nutritional stress may also lead to an increase in protectiveness by baboon mothers. We therefore hypothesized that, relative to controls, NR mothers will exhibit more time in contact with infants, less time out of arm’s reach, and higher rates of infant restraint.

Materials and Methods

Humane Care Guidelines

The study animals were housed in two intact social groups at The Texas Biomedical Research Institute (TBRI), formerly the Southwest Foundation for Biomedical Research. Each group consisted of 1 vasectomized male and up to 16 females per cage (3.5m high with a floor area of 37m2); social grouping and feeding procedures have been described in detail elsewhere [67]. Briefly, once daily all animals were transferred to individual feeding cages for a 2-hour period where they were fed a controlled diet of Purina Monkey Diet 5038 biscuits. Control animals (N = 8) were fed ad libitum, while NR females (N = 11) were fed 70% of feed consumed by controls on a weight-adjusted basis throughout the study period [68]. All procedures were approved by the TBRI Institutional Animal Care and Use Committee and conducted in facilities approved by the Association for Assessment and Accreditation of Laboratory Animal Care.

Maternal Behavior

Beginning 8 weeks prior to the expected date of parturition the behavior of each pregnant socially-housed female was recorded with a handheld video for three 20-minute sample periods per week whenever possible. Video collection continued until the infant reached 12 weeks of age (416 observations, 139 hours total). Care was taken to ensure that observation samples were equally distributed between morning and afternoon hours. All videotaped observations were subsequently coded by the first author (LEOL) using The Observer Video-Pro® (Noldus Information Technology Inc., Leesburg, VA).

Activity level was measured by the percent time per observation period the subject spent engaged in walking, running, climbing, hanging, or fighting states; due to the infrequency or short duration of many of these behaviors, all active behaviors were also combined into a general “active" category. All other states were categorized as “inactive” behaviors, including sitting, laying down, and sleeping. Social behaviors were defined following Ramirez [60] and include the percent time engaged in social grooming (either as the recipient or groomer), the rate per minute observed of affiliative events (e.g., approach, attempt touch, embrace, enlist groom, groom other, huddle, inspect genitals, muzzle/muzzle, present, touch, receive affiliative behavior from other), and the rate per minute observed of aggressive behaviors (e.g., bite, display, fight, hit, lunge, open mouth, pull, pull hair, round mouth, stare, yawn, receive aggressive behavior from other). Rates of receiving aggression from others were also analyzed separately. Following Bardi, French, Ramirez and Brent [65], SDB include scratch self, muzzle wipe, brow wipe, and mantle shake. Stereotypical self-directed behaviors (e.g., pull/eat own hair, head toss, clasping own body, suck self, other abnormal behavior) were also included in the ethogram but were rarely observed (n = 8) and therefore excluded from the analyses. All behavioral categories were analyzed as behavioral category aggregates as well as individual behaviors.

Mother-Infant Interactions

Maternal behavioral was coded based on categories developed by Ramirez [60] and included two main dimensions: interaction behaviors and proximity. Mother-infant interaction behaviors included break contact, dangle, detach infant, drag infant, keep from nursing, make contact, restrain infant, retrieve infant, and rough handling. Rejection was categorized as breaking contact, detaching infant, and keeping infant from nursing. Protective behaviors included make contact, restrain infant, and retrieve infant. Mother-infant proximity was categorized as ventral contact, dorsal contact, inappropriate contact, other contact, within arm’s reach, or greater than arm’s reach. Different forms of contact (ventral, dorsal, inappropriate, and other) were then aggregated and proximity was analyzed as in contact, within arm’s reach, or greater than arm’s reach. Proximity and several mother-infant interaction behaviors (including dangle, drag infant, restrain infant, retrieve infant, and rough handling) were recorded as states and calculated as percent time per observation, while all other behaviors were recorded as events and calculated as rate per minute observed. Infants were expected to transition from dependence to independence during the postpartum observation period. Consequently, the postpartum period was divided into three four-week sub-periods (weeks 1-4, 5-8, and 9-12).

Dominance Coding and Infant Sex

We examined the effects of dominance on both female behavior and mother-infant interactions with a dominance hierarchy established for each cage prior to the onset of detailed behavioral observations following methods described by Bramblett [69]. We also included the sex of the infant when analyzing rates of protective behaviors. However, because neither dominance nor sex of the infant resulted in any significant effects, these analyses are not presented.

Statistical Analysis

Statistical analyses were performed using SPSS® statistical software to identify statistically significant differences due to time, treatment group (control vs. NR), and their interaction. Effect sizes were also calculated using eta. Event frequency rates per minute were calculated for all event behavior categories. Durations of active and inactive behaviors as well as social grooming were calculated as percentages of total time. Prenatal, postpartum, and overall means for each behavior were calculated for all subjects. Repeated measures ANOVAs were then used to simultaneously test for the effects of treatment group, time (prenatal vs. post-partum or age of infant), and the interaction between treatment group and time. The significance level for all tests was set at a two-tailed alpha level of p ≤ 0.05 (indicated in figures and captions as *).

Results

Female Behavior

Activity level

Activity level (the percent time per observation the subject spent engaged in walking, running, climbing, hanging, or fighting states) did not differ between the prenatal and post-partum periods (p > 0.05) (Table 1). Activity level did not differ between control females and NR females (p > 0.05). The interaction between treatment and maternal condition did not affect activity level (p > 0.05).

Table 1.

Female Behavior Results

Categorical comparison (value ± SE)
Prenatal Post-partum
Effect of parturition
Active 4.81% ± 0.66% 5.01% ± 0.54%
Affiliative 0.510/min ± 0.04 1.113/min ± 0.10
Aggressive 0.030/min ± 0.01 0.066/min ± 0.01
 Rec aggression 0.009/min ± 0.00 0.024/min ± 0.00
SDB 1.067/min ± 0.07 0.631/min ± 0.06
 Scratch self 0.606/min ± 0.05 0.336/min ± 0.05
Categorical comparison (value ± SE)
Control NR
Effect of treatment
Activity 4.6% ± 0.8% 5.2% ± 0.8%
Affiliative 0.916/min ± 0.08 0.706/min ± 0.08
Aggression 0.064/min ± 0.01 0.032/min ± 0.01
 Rec aggression 0.023/min ± 0.00 0.012/min ± 0.00
SDB 0.987/min ± 0.07 0.711/min ± 0.07
 Scratch self 0.569/min ± 0.06 0.372/min ± 0.06
Categorical comparison (value ± SE)
Control NR
Interaction of parturition and treatment
Activity
 prenatal 4.2% ± 1.0% 5.3% ± 0.1%
 post-partum 5.0% ± 0.1% 5.0% ± 0.1%
Affiliative
 prenatal 0.563/min ± 0.05 0.457/min ± 0.05
 post-partum 1.269/min ± 0.14 0.956/min ± 0.13
Aggression
 prenatal 0.044/min ± 0.02 0.017/min ± 0.01
 post-partum 0.084/min ± 0.01 0.047/min ± 0.01
Rec aggression
 prenatal 0.013/min ± 0.00 0.006/min ± 0.00
 post-partum 0.032/min ± 0.01 0.018/min ± 0.01
SDB
 prenatal 1.277/min ± 0.10 0.857/min ± 0.09
 post-partum 0.696/min ± 0.09 0.566/min ± 0.09
Scratch self
 prenatal 0.761/min ± 0.07 0.450/min ± 0.07
 post-partum 0.377/min ± 0.08 0.295/min ± 0.07
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Affiliative behavior

Affiliative behavior was significantly higher after the birth of an infant (F(1,13) = 41.417, p ≤ 0.001, eta = 0.87) (Figure 1A). Rates of affiliative behaviors did not differ between control females and NR females (p > 0.05). The interaction between treatment and maternal condition did not affect rates of affiliative behaviors (p > 0.05).

Figure 1. Rates per minute of female behaviors.

Figure 1

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1A Rates of affiliative behaviors; 1B Rates of aggressive behaviors; and 1C Rates of self-directed behaviors. Data are means, with one standard error of the mean (SEM) represented by vertical bars. Control N = 7, NR N = 8. *There was a significant effect of parturition on prenatal and post-partum means (p ≤ 0.05; repeated measures ANOVA). ** There was a significant effect of treatment group between control and NR females (p ≤ 0.05; repeated measures ANOVA). † While the interaction between parturition and treatment group only approached significance (p ≤ 0.1; repeated measures ANOVA), during the prenatal period control females exhibited higher rates of SDB than NR females (p ≤ 0.05; one-way ANOVA).

Aggression

Aggression was significantly higher after the birth of an infant (F(1,13) = 6.934, p = 0.021, eta = 0.59) (Figure 1B). There was a significant simple main effect of treatment group on rates of aggressive behavior (F(1,13) = 5.705, p = 0.033, eta = 0.55) with control females exhibiting higher rates than NR females. The interaction between treatment group and maternal condition did not affect rates of aggressive behavior (p > 0.05).

Rates of receiving aggression were higher after the birth of an infant (F(1,13) = 11.318, p = 0.005, eta = 0.68). Rates of receiving aggression between control and NR females approached significance (F(1,13) = 3.285, p = 0.093, eta = 0.202) with control females receiving aggression more frequently compared to NR females. The interaction between treatment group and maternal condition did not affect rates of receiving aggression (p > 0.05).

Self-directed behaviors (SDB)

Self-directed behaviors (SDB) were significantly lower after the birth of an infant (F(1,13) = 30.779, p ≤ 0.001, eta = 0.84) (Figure 1C). There was a significant simple main effect of treatment group on SDB rates (F(1,13) = 7.359, p = 0.018, eta = 0.60) with control females exhibiting higher rates than NR females. The interaction between treatment group and maternal condition on rates of SDB only approached significance (F (1,13) = 3.385, p = .089, eta = 0.45). Post-hoc analysis revealed a significant difference in SDB rates between control and NR females during the prenatal period (F(1,16) = 16.428, p = 0.001) with control females exhibiting higher rates than NR females.

Within SDB behaviors, there was also a significant decrease in rates of self-scratching (F(1,13) = 17.435, p = 0.001, eta = 0.76). There was a significant simple main effect of treatment group on scratch self (F(1,13) = 6.036, p = 0.029, eta = 0.56) with control females exhibiting higher rates than NR females. The interaction between treatment group and maternal condition only approached significance for scratch self (F(1,13) = 3.158, p = 0.099, eta = 0.44). Post-hoc analysis revealed a significant difference between control and NR females during the prenatal period (F(1,16) = 16.428, p = 0.001) with control females exhibiting higher rates than NR females (Figure 2).

Figure 2. Rates per minute of individual SDB during the prenatal period.

Figure 2

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Data are means, with one SEM represented by vertical bars. † While the interaction between parturition and treatment group only approached significance (p ≤ 0.1; repeated measures ANOVA), during the prenatal period NR mean value was significantly lower from that of the control group for rates of scratch self (p ≤ 0.05; one-way ANOVA).

Mother-infant interactions

Protective behavior

There was no effect of infant age for protective behaviors in aggregate (make contact, restrain infant, and retrieve infant), make contact, or restrain infant (p > 0.05). However, rates of females retrieving infants approached significance (F(2,18) = 2.908, p = 0.080, eta = 0.49) (Table 2). There were no significant differences in protective behaviors between control and NR mothers for aggregated protective behavior, make contact, restrain infant, or retrieve infant (p > 0.05). The interaction between NR and infant age did not affect protective behavior in aggregate, make contact, or restrain infant (p > 0.05). However, our results indicate a trend in the interaction between NR and infant age for rates of retrieving infants (F(2,18) = 2.863, p = 0.083, eta = 0.49). Post-hoc analysis indicated that control and NR females differed significantly from each other during weeks 5-8 (one-way between subjects ANOVA: F(1,13) = 7.200, p = 0.019) (Figure 3).

Table 2.

Mother-Infant Interaction Results

Categorical comparison (value ± SE)
Weeks 1-4 Weeks 5-8 Weeks 9-12
Effect of infant age
Protective behavior 0.169/min ± 0.06 0.497/min ± 0.12 0.448/min ± 0.27
Make Contact 0.089/min ± 0.03 0.270/min ± 0.07 0.241/min ± 0.13
Restrain Infant 0.059/min ± 0.03 0.169/min ± 0.05 0.177/min ± 0.12
Retrieve Infant 0.021/min ± 0.01 0.059/min ± 0.01 0.030/min ± 0.02
Time in Contact 90.3% ± 2.3% 69.5% ± 5.4% 57.3% ± 6.1%
Within AR 5.6% ± 1.9% 16.1% ± 3.6% 20.2% ± 6.3%
Greater than AR 4.0% ± 1.4% 14.3% ± 4.5% 22.3% ± 4.2%
Categorical comparison (value ± SE)
Control NR
Effect of treatment
Protective behavior 0.458/min ± 0.22 0.285/min ± 0.17
Make Contact 0.261/min ± 0.12 0.139/min ± 0.09
Restrain Infant 0.148/min ± 0.10 0.122/min ± 0.07
Retrieve Infant 0.049/min ± 0.02 0.024/min ± 0.01
Time in Contact 67.8% ± 6.0% 76.9% ± 4.5%
Within AR 14.2% ± 5.8% 13.8% ± 4.4%
Greater than AR 17.9% ± 4.5% 9.2% ± 3.4%
Categorical comparison (value ± SE)
Control NR
Interaction of treatment and infant age
Protective behavior
 weeks 1-4 0.213/min ± 0.09 0.125/min ± 0.07
 weeks 5-8 0.695/min ± 0.19 0.300/min ± 0.15
 weeks 9-12 0.465/min ± 0.43 0.431/min ± 0.32
Make Contact
 weeks 1-4 0.124/min ± 0.05 0.054/min ± 0.04
 weeks 5-8 0.381/min ± 0.11 0.158/min ± 0.09
 weeks 9-12 0.277/min ± 0.21 0.205/min ± 0.16
Restrain Infant
 weeks 1-4 0.061/min ± 0.04 0.057/min ± 0.03
 weeks 5-8 0.220/min ± 0.08 0.117/min ± 0.06
 weeks 9-12 0.162/min ± 0.19 0.191/min ± 0.14
Retrieve Infant
 weeks 1-4 0.028/min ± 0.01 0.013/min ± 0.01
 weeks 5-8 0.094/min ± 0.02 0.025/min ± 0.02
 weeks 9-12 0.026/min ± 0.03 0.035/min ± 0.02
Time in Contact
 weeks 1-4 84.8% ± 3.7% 95.9% ± 2.8%
 weeks 5-8 61.0% ± 8.6% 78.0% ± 6.5%
 weeks 9-12 57.7% ± 9.8% 56.9% ± 7.4%
Within AR
 weeks 1-4 7.5% ± 3.1% 3.7% ± 2.3%
 weeks 5-8 17.9% ± 5.8% 14.2% ± 4.4%
 weeks 9-12 17.1% ± 10.1% 23.3% ± 7.6%
Greater than AR
 weeks 1-4 7.7% ± 2.2% 0.4% ± 1.7%
 weeks 5-8 21.0% ± 7.2% 7.6% ± 5.4%
 weeks 9-12 24.9% ± 6.7% 19.7% ± 5.1%
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Figure 3. Rates of retrieve infant.

Figure 3

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Data are means, with one SEM represented by vertical bars. † While the interaction between infant age and treatment group only approached significance (p ≤ 0.1; repeated measures ANOVA), NR mean value was significantly lower from that of the control group for weeks 5-8 (p ≤ 0.05; one-way ANOVA; control N = 4, NR N = 7).

Proximity

Time spent in contact decreased significantly as infants increased in age (F(2,18) = 18.700, p ≤ 0.001, eta = 0.82) (Figure 4A). Time spent within arm’s reach increased (F(2,18) = 6.633, p = 0.007, eta = 0.65), and time spent at greater than arm’s reach increased significantly (F(2,18) = 10.454, p = 0.001, eta = 0.73) (Figure 4B). There were no significant differences between control and NR mothers for time spent in contact, time spent within arm’s reach, or time spent at greater than arm’s reach (p > 0.05). The interaction between NR and infant age did not affect time spent in contact, within arm’s reach, or at greater than arm’s reach (p > 0.05).

Figure 4. Rates of mother-infant interaction behaviors.

Figure 4

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4A Proportion of time mothers spent in contact with infants, 4B Proportion of time infants spent at distances greater than arms reach from their mothers. Data are means, with one SEM represented by vertical bars. Control N = 4, NR N = 7. *There was a significant effect of age of infant on time spent in contact, time spent within arm’s reach (not shown), and time spent at greater than arm’s reach (p ≤ 0.05; repeated measures ANOVA). Offspring of control females spend more time at greater distance during all periods, though in no case did this difference approach significance (p ≥ 0.05; repeated measures ANOVA).

Discussion

Parturition and female behavior

As expected, parturition affected female behavior with rates of affiliative and aggressive behaviors increasing after the birth of the infant. Our results are consistent with previous studies in regards to the effects of parturition on social behavior. Specifically, females with infants received more social attention, increasing affiliative and aggressive interactions, including receiving aggression from other individuals. SDB rates decreased after parturition, contrary to the findings of a previous study with this species at this facility [41]. However, Brendt et al. [41] suggest that the difference in rates between the two periods in their study may be the result of a suppression of SDB in the prenatal period rather than an increase during the postpartum period. Females in our study were fed in individual enclosures, eliminating feeding competition and likely decreasing the amount of psychosocial stress factors that might affect SDB rates.

Nutritional regime and female behavior overall

Overall, there were no observed differences in activity level due to treatment group, contrary to our prediction that NR females would show higher activity levels than control females. However, it is important to note that activity levels among all study subjects were consistently very low with activity rates averaging only 5% of the time observed and ranging from 2-10% of the time. While previous studies of NR in Old World primates have shown increased levels of activity as a result of NR [57], these were studies that were using socially housed but also socially fed primate groups. Vitousek and colleagues [39] have suggested that the increased activity levels reported by Weed and colleagues [57] are due to intense activity prior to feeding times and in fact mask overall lower activity rates throughout the rest of the day.

While rates of affiliative behaviors rose significantly following the birth of the infant as expected, no differences were detected between treatment groups. Rates of aggression were higher in control females, contrary to our prediction that NR females would engage in higher rates of aggressive behaviors. Nevertheless, the very low levels of both affiliative and aggressive behaviors observed may be the result of the very low activity levels in general. Aggressive behaviors and affiliative behaviors in the context of reconciliation are frequently associated with feeding competition, particularly in free-ranging animals [71, 72]; our study protocol eliminated this motivation for social interaction. Notably, the lack of differences in aggressive behaviors between control and NR females are not consistent with Huber et al.’s suggestion that that increased aggression in IUGR offspring might be the result of socially learned behaviors acquired early in life.

Contrary to expectations, NR females had significantly lower SDB rates than controls. If pregnancy is a period of relative anxiety, then this result may indicate that the typical behavioral response to prenatal psychosocial stress is suppressed in NR females. Indeed, our results for control females are similar to other studies with the same species (Papio sp.) conducted at TBRI, where females exhibited prenatal self-scratching rates at 0.817/minute [41], suggesting that control females engage in SDB at rates typical for this study population. It is also possible that the lower rates of SDB among NR females are a strategic optimization of energy use. It has been suggested that displacement behaviors such as SDB provide a behavioral coping strategy through which individuals can lessen the physiological response to anxiety [73]. Yet such behaviors require energetic output. Individuals who are not energetically taxed may benefit from engaging in SDB to minimize the glucocorticoid output while energetically stressed individuals may forego such behaviors to minimize energy use, increasing glucocorticoid output but maximizing energy available for offspring development. Despite research demonstrating an increase in fetal cortisol due to nutrient restriction, our research team did not find significant differences in maternal cortisol among this study group [34], suggesting that SDB was not an effective means of mitigating glucocorticoid output. Therefore, it is more likely that SDB are reduced in NR females during pregnancy due to decreased available energy.

As mentioned above, the differences in activity rates in the current study were not statistically significant; however, in previous work by our team using the same model of NR and the same species, activity levels derived from accelerometers attached to the animals’ collars revealed significant differences in activity levels even in the absence of clear differences in activity budgets [31]. Those results suggest that accelerometers may record inconspicuous, but metabolically important, movements. SDB may fit this definition. In other words, eliminating subtle activities may yield adaptively significant energetic savings that protect fetal growth during NR [31].

Nutrition restriction and maternal behavior

The second aim of this project was to determine if NR led to significant differences in mother-infant interactions and maternal style. While we found no significant differences in protective behaviors across the entire study period, we did find a decrease in the percentage of time mothers spent in contact with infants, as expected. In the wild, two months after birth marks an important stage in infant development, with infants traveling independently and engaging in more social interactions at this age [74, 75]. Furthermore, our data show clear trends with NR mothers spending more time in contact with infants and infants of NR females closer to their mothers.

In the absence of other clear differences in female behavior post-partum, we attribute the noticeable trends in contact and proximity to differences in activity rates of the infants born to NR females – presumably lower due to energetic deficits – rather than to differences in maternal style. Therefore, we reason that well-fed infants are more interested in leaving their mothers while those who are nutritionally taxed remain in contact with their mothers [76–78]. A second possibility is that the trends in contact and proximity between control and NR subjects is due to differences in offspring temperament, as has been documented in IUGR offspring of both rodents and sheep [9, 10] and in nonhuman primate studies investigating the effects of differences in available milk energy and cortisol in mother’s milk [78–80]. Our team also found less motivation in IUGR offspring during adolescence [8], which may also lead to more time spent in close proximity to mothers during infancy.

In conclusion, NR resulted in lower rates of aggressive behaviors and lower rates of SDB, particularly during the prenatal period. However, because rates of activity were lower than expected, confirming our findings would require further research with an expanded sample size. Nutrient restriction clearly influenced rates of SDB. It is possible that moderate global NR prompts an adaptive suppression of SDB in pregnant female baboons as a means of mitigating the insult of NR on fetal development.

Furthermore, our findings suggest that maternal-infant interactions are influenced by NR in regards to contact between the mother and infant, but any future studies should consider the role of the infant in determining mother-infant behavior. One limitation of our own study was the use of handheld video to conduct behavioral data collection. As the mother was the study subject, infants often left the field of view for long periods. One remedy for this during future projects would be to focus on the infant during behavioral data collection. By doing so, one could analyze the infant’s role in maintaining proximity. Once moving independently from the mother, infants are active independent agents and should thus be considered as equally contributing to mother-infant interactions, rather than viewed as passive entities whose behaviors are shaped solely by the constraints of maternal style.

Acknowledgments

This research was supported by NICHD-021350 and HD 21350. The project described was supported by Award Number R21HD057480 from the Eunice Kennedy Shriver National Institute of Child Health &Human Development. The content is solely the responsibility of the authors and does not necessarily represent the official views of the Eunice Kennedy Shriver National Institute of Child Health & Human Development or the National Institutes of Health. This research was also supported by a grant from San Antonio Life Sciences Institute.

We would like to thank Michael Bauman, Jesse Rodriguez, Katie Smith, Heath Neville, William Ramirez, Meghan Egan, and Stephanie Ramirez for assistance on this project.

Supported by: NICHD-021350 and HD 21350

Footnotes

DR. LYDIA E. O. LIGHT (Orcid ID : 0000-0001-9791-3487)

DR. THAD QUINCY BARTLETT (Orcid ID : 0000-0001-5994-9454)

DR. HILLARY FRIES HUBER (Orcid ID : 0000-0001-9734-427X)

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