Thad Q. Bartlett

Intragroup and Intergroup Social Interactions in White-Handed Gibbons

One of the least studied aspects of the Hylobatidae is their social behavior. In the past, researchers have attributed this to a general lack of affiliative social interactions due to small group size and the hostile nature of intergroup encounters. Data collected on white-handed gibbons (Hylobates lar) in Khao Yai National Park, Thailand, indicate that gibbons engage in higher rates of social behavior than had previously been appreciated. In addition to relatively high rates of intragroup social contact, gibbons engaged in social behavior, including play and grooming, with members of neighboring groups. These findings obligate a renewed consideration of the nature and function of territoriality in primates.

Poor nutrition during pregnancy and lactation negatively affects neurodevelopment of the offspring: evidence from a translational primate model

BACKGROUND Studies of the effects of prenatal nutrition on neurodevelopment in humans are complicated because poor nutrition occurs in the context of psychosocial stressors and other risk factors associated with poor developmental outcomes. OBJECTIVE Under controlled experimental conditions, we tested an effect of prenatal nutrition on neurodevelopmental outcomes in the nonhuman primate. DESIGN Juvenile offspring of 19 female baboons, whose diets were either restricted [maternal nutrition restriction (MNR)] or who were fed ad libitum (control), were administered the progressive ratio task from the Cambridge Neuropsychological Test Automated Battery. Activity, persistence, attention, and emotional arousal were coded from videotapes. These established, reliable methods were consistent with those used to assess individual differences in the behaviors of school-age children. RESULTS MNR offspring (3 female and 4 male offspring) had significantly fewer responses and received fewer reinforcements on the progressive ratio task than did control offspring (8 female and 4 male offspring). MNR offspring showed a more variable activity level and less emotional arousal than did control offspring. Female MNR offspring showed more variable and lower levels of persistence and attention than did female control offspring. Thus, under controlled experimental conditions, data support a main effect of prenatal nutrition on highly translatable neurodevelopmental outcomes. CONCLUSIONS Nutritional interventions during pregnancy have been successfully used to target neurodevelopmental problems, such as increasing folic acid intake during pregnancy to decrease the incidence of neural tube defects. Results from the current study can be used to support the testing of nutritional preventive interventions for the most-common childhood behavior problems.

Prenatal betamethasone exposure has sex specific effects in reversal learning and attention in juvenile baboons

OBJECTIVE We investigated effects of 3 weekly courses of fetal betamethasone (βM) on motivation and cognition in juvenile baboon offspring utilizing the Cambridge Neuropsychological Test Automated Battery. STUDY DESIGN Pregnant baboons (Papio species) received 2 injections of saline control or 175 μg/kg βM 24 hours apart at 0.6, 0.65, and 0.7 gestation. Offspring (saline control female, n = 7 and saline control male, n = 6; βM female [FβM], n = 7 and βM male [MβM], n = 5) were studied at 2.6-3.2 years with a progressive ratio test for motivation, simple discriminations and reversals for associative learning and rule change plasticity, and an intra/extradimensional set-shifting test for attention allocation. RESULTS βM exposure decreased motivation in both sexes. In intra/extradimensional testing, FβM made more errors in the simple discrimination reversal (mean difference of errors [FβM - MβM] = 20.2 ± 9.9; P ≤ .05), compound discrimination (mean difference of errors = 36.3 ± 17.4; P ≤ .05), and compound reversal (mean difference of errors = 58 ± 23.6; P < .05) stages as compared to the MβM offspring. CONCLUSION This central nervous system developmental programming adds growing concerns of long-term effects of repeated fetal synthetic glucocorticoid exposure. In summary, behavioral effects observed show sex-specific differences in resilience to multiple fetal βM exposures.

Sex-Dependent Cognitive Performance in Baboon Offspring Following Maternal Caloric Restriction in Pregnancy and Lactation

In humans a suboptimal diet during development has negative outcomes in offspring. We investigated the behavioral outcomes in baboons born to mothers undergoing moderate maternal nutrient restriction (MNR). Maternal nutrient restriction mothers (n = 7) were fed 70% of food eaten by controls (CTR, n = 12) fed ad libitum throughout gestation and lactation. At 3.3 ± 0.2 (mean ± standard error of the mean [SEM]) years of age offspring (controls: female [FC, n = 8], male [MC, n = 4]; nutrient restricted: female [FR, n = 3] and male [MR, n = 4]) were administered progressive ratio, simple discrimination, intra-/extra-dimension set shift and delayed matching to sample tasks to assess motivation, learning, attention, and working memory, respectively. A treatment effect was observed in MNR offspring who demonstrated less motivation and impaired working memory. Nutrient-restricted female offspring showed improved learning, while MR offspring showed impaired learning and attentional set shifting and increased impulsivity. In summary, 30% restriction in maternal caloric intake has long lasting neurobehavioral outcomes in adolescent male baboon offspring.

Metabolic adjustments to moderate maternal nutrient restriction

Reduced food availability in pregnancy influences fetal growth, obstetric outcomes and offspring health in both developing and developed countries. The objective of the present study was to determine responses to moderate global maternal nutrient restriction (MNR) during pregnancy in baboons (Papio hamadryas) - an established non-human primate model for pregnancy-related research. Starting at 30 d gestation (dG), twelve pregnant baboons received 70 % of food (MNR group) consumed by twenty ad libitum-fed pregnant controls. Maternal body weight, BMI, food intake and physical activity were measured before pregnancy, at 90 dG and at 165 dG (full-term 180 dG). Fetal and placental weights were recorded at the time of Caesarean section (90 and 165 dG). Activity patterns were also evaluated in fourteen non-pregnant female baboons. Behavioural observations were made in five non-pregnant, six control and four MNR animals. Pregnant baboons decreased overall physical activity and energy-expensive behaviours compared with non-pregnant baboons. In the MNR group, maternal weight, weight gain and maternal physical activity were reduced compared with the control animals. MNR decreased placental weight and volume compared with control, while fetal weight and length were unaffected. We conclude that decreased physical activity and increased usage of maternal available body stores play an important role in the maternal response to pregnancy. Also, adaptations in maternal behaviour and energy utilisation protect fetal growth during moderate MNR.

Performance of juvenile baboons on neuropsychological tests assessing associative learning, motivation and attention

The CANTAB (Cambridge Neuropsychological Test Automated Battery), a system developed for human neuropsychological testing, has previously been used to assess cognitive function in two species of nonhuman primates, common marmoset monkeys and rhesus macaques. We describe the application of the system to the juvenile baboon, a nonhuman primate species offering specific investigative advantages. Juvenile baboons were trained and tested on a progressive ratio task to assess motivation, simple discrimination and simple reversal tasks to assess associative learning, and intra- and extra-dimensional set-shifting tasks to assess selective attention and attentional set-shifting, respectively. Study subjects were 8 juvenile baboons (Papio sp.), 4 females and 4 males aged 3.0+/-0.1 (mean+SEM) years and weight 8.2+/-0.4 kg. All baboons were easily trained, readily learned the neuropsychological tests and exhibited a stable performance. Applying a method such as the CANTAB has significant implications for expanding on the translational utility of the baboon in studies of neurodevelopment.

CANTAB delayed matching to sample task performance in juvenile baboons.

This study reports the administration of the Cambridge Neuropsychological Test Automated Battery systems delayed matching to sample (DMTS) task to juvenile baboons. Nine subjects (female=5, male=4) were trained with delay intervals ranging from 0 to 80s. Trial unique stimuli were utilized in combination with matching to sample, in contrast to non-matching to sample, to more accurately assess components of medial temporal lobe (hippocampal formation) mediated working memory. These parameters force subjects to rely on recognition for matching stimuli and overcome their innate tendency to choose novel stimuli (non-matching), thus increasing task difficulty. Testing with delays intervals of 0-2, 4, 8, and 16s revealed decreased percent correct responding as delay intervals increased. An effect of 1 vs. 3 distractor stimuli on accuracy was also noted. Increasing the number of distractors resulted in decreased observing response latencies. The increase in choice response latency seen with increasing delay interval was independent of number of distractor stimuli presented. There were no sex differences in task performance. Our laboratory is focused on understanding the functional consequences of suboptimal conditions during pregnancy and early postnatal life in offspring. The ability of juvenile baboons to perform the DMTS task demonstrates the utility of this non-human primate model in examining pre- and post-natal conditions that impact the development of working memory. Evaluation of causes and consequences of impaired working memory in a variety of human diseases will be assisted by the use of this task in nonhuman primate models of human health and disease.

Seasonal Home Range Use and Defendability in White-Handed Gibbons (Hylobates lar) in Khao Yai National Park, Thailand

Gibbons are unique among hominoids in that they form small, socially monogamous groups that defend stable home ranges against encroachment by neighboring conspecifics. The evolution of this combination of traits, and the role of foraging ecology in its emergence, has long been the subject of speculation and research (Leighton 1987; Chivers 2001; Bartlett 2007). Early models focused on the highly frugivorous diets of gibbons and the consequent inability of adult females to share feeding resources. Social and reproductivemonogamy, it was argued, resulted from the inability of males to defend areas large enough to support more than one adult female and her offspring. While males of monogamous species might willingly associate with multiple females (and experience increased reproductive success as a result), the distribution of females into separate territories was thought to limit a male’s ability to defend access to more than one female, leaving males no other option but to travel with a single female at a time (Ellefson 1974; Emlen and Oring 1977; Wrangham 1979; Raemaekers and Chivers 1980; Leighton 1987). According to van Schaik and Dunbar (1990), one weakness of this model as applied to gibbons is that long daily path lengths (DPL) relative to home range size in most populations indicate that gibbon males could readily defend the territories of multiple females simultaneously. Based largely on these finding, van Schaik and Dunbar reject what they refer to as the female dispersion model, paving the way for alternative explanations for social monogamy in gibbons that highlight the role of sexual competition [e.g., infanticide prevention (van Schaik and Dunbar 1990) and mate guarding (Palombit 1999)] rather than ecological selection pressures (but see Brockelman 2005, this volume). However, in my view, the rejection of the female dispersion model is premature.

Understanding stable bi-female grouping in gibbons: feeding competition and reproductive success

IntroductionSpecies of the order Primates are highly gregarious with most species living in permanent heterosexual social groups. According to theory in socioecology maximum social group size is limited by rates of intra-group feeding competition and associated increases in travel costs. Unlike other hylobatids, which are predominantly pair living, cao vit gibbons (Nomascus nasutus), and two other species of crested gibbon (Nomascus spp.) living in northern seasonal forest, regularly exhibit larger bi-female groups. To better understand the ability of northern gibbons to live in stable bi-female groups, we examined food distribution, feeding competition and reproductive success over a period of six years in a small cao vit gibbon population at Bangliang, Guangxi, China.ResultsIn general, we found weak evidences for within-group contest or scramble competition in our two study groups, which we attribute to high spatial and temporal heterogeneity in the distribution of their important food species. Nevertheless, the larger of the two groups studied increased feeding time and group spread during lean periods, factors that may limit cao vit gibbon group size to a maximum of two breeding females. Relative to tropical pair-living gibbons, there is no evidence that cao vit gibbons travel farther or spend more time feeding, but they did consume more leaves and buds and less fruit and figs. Despite their highly folivorous diet, the average inter-birth interval is comparable to tropical gibbon populations, and the survival rate of infants and juveniles in our study groups is high.ConclusionCao vit gibbons do not suffer obvious costs in terms of feeding competition and reproductive success by living in bi-female groups, but within-group feeding competition may determine the upper the limit of cao vit gibbon group size to a maximum of two breeding females. These findings contribute to a growing body of evidence that bi-female grouping can be a stable grouping pattern of gibbons in certain habitats and further emphasize the flexibility of gibbon social organization.

Feeding Postures of Cao Vit Gibbons (Nomascus nasutus) Living in a Low-Canopy Karst Forest

Food acquisition is an important factor in the evolution of primate postural behavior. Gibbons are well known for their ability to exploit terminal branches by means of below branch suspensory feeding, but few studies of gibbon positional behavior have been conducted since the seminal work of the 1970s and 1980s. We studied the feeding posture of three cao vit gibbon groups living in degraded karst forest in Bangliang Gibbon Nature Reserve between August 2008 and December 2009 to determine if body mass, age, and food type affect feeding posture. We found that cao vit gibbons spent most of their time feeding from branches (59.4 %) and twigs (33.2 %) in the middle canopy of the forest (5–10 m). They used suspensory hanging and sitting as their main feeding postures. Large-bodied gibbons spent more time on larger supports than smaller juveniles when feeding on nonfig fruit and leaves. In addition, gibbons of all age–sex classes adopted a suspensory posture more often when using smaller (twigs) or more flexible (lianas) supports. We found little evidence of age–sex differences in the frequency of suspensory feeding. The subtle differences we did detect suggest that intragroup feeding competition or ontogeny may confound the body size effects on feeding posture. Overall our findings conform to the view that within species positional behavior is largely constrained by musculoskeletal anatomy and not by habitat quality because cao vit gibbons showed a similar pattern of canopy and substrate use to gibbons occupying less disturbed forests.