Population densities of Hylobates agilis in forests with different disturbance histories in Ulu Muda Forest Reserve, Malaysia.

Small ape habitat throughout Malaysia is rapidly being lost, degraded, and fragmented, and the effects of these changes on the abundance on this taxon are currently unknown. This study assessed the group density of Hylobates agilis in virgin forest, previously logged forest (1960s-1990s), and recently logged forest (2015-2017) of the Ulu Muda Forest Reserve (UMFR), Kedah, Malaysia. We conducted fixed-point active acoustic triangulation at nine survey areas to estimate group density. We used vegetation "speed plots" and satellite imagery to quantify habitat characteristics and used model selection to identify ecological predictors of group density variation. The estimated group density of H. agilis in UMFR was 4.03 ± 0.14 groups km-2 , with an estimated total of 2927 ± 102 groups in areas below 450 m a.s.l. in UMFR. Group density did not differ significantly among habitat types. The best ecological predictors for group density were canopy cover and proportion of deforested area. Areas with recent deforestation were associated with relatively high group densities, suggesting compression of the populations persisting in these habitat types. The consistently high group densities detected in all forest types emphasizes the importance of degraded forest as habitat for H. agilis. Because of the threats to small apes in Malaysia, and the uncertain status of most populations, we recommend a nationwide population census and regular monitoring to inform conservation planning and implementation. Most urgently, we call for immediate and permanent protection of UMFR and other forests in the Greater Ulu Muda landscape to protect the globally significant populations of H. agilis, as well as other charismatic and threatened megafauna, birds, and flora in the area.

White-handed gibbons (Hylobates lar) alter ranging patterns in response to habitat type.

Small apes are often characterized as inhabiting small home ranges and being dependent on evergreen forest due to their dietary specialization on ripe fruits. Yet few primate studies, particularly those with gibbons, have considered intraspecific variations in ranging behaviors in response to local ecological conditions. This study examines Endangered white-handed gibbon (Hylobates lar) ranging patterns in a heterogeneous landscape. We conducted 13 months of behavioral observations on four white-handed gibbon groups living in Huai Kha Khaeng Wildlife Sanctuary in western Thailand, and combine these data with group location and transect-based productivity data. We compare home range area, site fidelity, and microhabitat preferences. Home range (HR) area varied considerably among the four groups (17-61 hectares). Site fidelity was higher in one of the groups with more evergreen forest in the HR (0.72 ± 0.1) than one of the groups with very little evergreen forest in the habitat (0.47 ± 0.07). While groups with more evergreen forest in the HR preferred evergreen forest areas, groups with very little evergreen forest within the HR demonstrated less preference for evergreen forest areas. We conclude that gibbons at this site exhibit a considerable degree of behavioral variation in response to local ecological conditions. These findings suggest that while gibbons exhibit significant ecological flexibility, this flexibility may be limited by habitat type and key food resources.

Are social media reports useful for assessing small ape occurrence? A pilot study from Peninsular Malaysia.

Citizen science-based research has been used effectively to estimate animal abundance and breeding patterns, to monitor animal movement, and for biodiversity conservation and education. Here, we evaluate the feasibility of using social media observations to assess the distribution of small apes in Peninsular Malaysia. We searched for reports of small ape observations in Peninsular Malaysia on social media (e.g., blogs, Facebook, Instagram, Twitter, YouTube, iNaturalist, etc.), and also used online, radio, print messaging, and word of mouth to invite citizen scientists such as birders, amateur naturalists, hikers, and other members of the public to provide information about small ape observations made during their activities. These reports provided new information about the occurrence of all three species of small apes (Hylobates agilis, Hylobates lar, and Symphalangus syndactylus) in Peninsular Malaysia. Social media users reported observations of small apes in almost every state. Despite the fact that small apes are believed to occur primarily in the interior of large forested areas, most observations were from fairly small (<100 km2 ) forests near areas of high traffic and high human population (roads and urban areas). This suggests that most outdoor enthusiasts primarily visit well-traveled and easily accessible areas, which results in biased sampling if only incidental observations reported on social media are used. A more targeted approach specifically soliciting reports from citizen scientists visiting large, less-accessible forests may result in better sampling in these habitats. Social media reports indicated the presence of small apes in at least six habitats where they had not been previously reported. We verified the reported data based on whether reports included a date, location, and uploaded photographs, videos and/or audio recordings. Well-publicized citizen science programs may also build awareness and enthusiasm about the conservation of vulnerable wildlife species.

Infant loss during and after male replacement in gibbons.

According to the sexual selection hypothesis, infanticide during resident male replacement is an adaptive strategy that has evolved because the killing of unweaned offspring sired by previous males shortens the inter-birth intervals of the mothers whose infants are targeted and thereby increases the reproductive fitness of the perpetrator. To test this hypothesis, we describe previously unreported cases of primary male replacement for two gibbon species (Hylobates lar and Nomascus nasutus), and review all other reported cases of primary male replacement in gibbons. Overall, infants were present in nearly half of all cases (16/33, 48%) and of the 18 infants present during replacement, 50% (N = 9) disappeared within 2 months of the event. In four of the five cases where there was sufficient demographic information to identify the likely sire of the subsequent offspring of females that lost infants, the new male was believed to be the sire. Infants were also less likely to die or disappear if the new male and original resident male were possible kin. However, there was no significant difference in the age of infants between those that died or disappeared following replacement and those that survived to weaning (p = .630). Our review of takeover-related infant loss in gibbons confirms that periods of male instability are risky for unweaned infants and that replacing males benefit from infant loss. Nevertheless, variability in the context of infant loss and difficulties related to data collection in the field make it difficult to test competing hypotheses concerning the mechanisms and functions of infanticide in the small apes.

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

BACKGROUND: We hypothesized that maternal nutrient restriction (NR) would increase activity and behavioral indicators of anxiety (self-directed behaviors, SDBs) 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 ≤ .018) and during the prenatal period (P ≤ .001) and engage in more aggressive behavior (P ≤ .033). Control females retrieved infants more than NR females during weeks 5-8 postpartum (P ≤ .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.

Long-term home range use in white-handed gibbons (Hylobates lar) in Khao Yai National Park, Thailand.

Ranging behavior is an important element of how nonhuman primates obtain sufficient resources to ensure biological maintenance and reproductive success. As most primates live in permanent social groups, group members must balance the benefits of group living with the costs of intragroup competition for resources. One way to mitigate the cost of intragroup feeding competition is to increase foraging-related travel, thereby increasing the number of patches visited. As a result we might expect home range size to increase as a function of group size. On the other hand, for perennially territorial species, ranging behavior may be constrained by the ranging requirements of territorial defense or by the location of neighboring territories, which would result in long-term stability in the size and location of a group's home range. In this study, we examined changes in range-use characteristics in one well-habituated group of white-handed gibbons (Hylobates lar) during three study periods over a 10-year span. Group size changed from five members, two adults, two juveniles, and one infant, in 1994, to two adults in 2002, and to three adults and one sub-adult in 2004. Despite inter-annual changes in core area use we found that home range location was highly stable across years. Nevertheless, home range size was larger and daily path length significantly longer in 2002 relative to 1994 when a dependent infant was present in the group. The percentage of time adults spent resting was also significantly greater in 1994 when the infant was present. These findings highlight the importance of considering group composition, in addition to group size, when evaluating the determinants of ranging behavior. We also consider the influence of individual and shared knowledge on home range stability.

Increased aggressive and affiliative display behavior in intrauterine growth restricted baboons.

BACKGROUND: We hypothesized intrauterine growth restricted offspring (IUGR) demonstrate higher rates of aggression and higher dominance ranks than control (CTR) offspring with normal weight at term; if aggressive behavior is advantageous during resource scarcity, developmental programming may lead to an association between aggression and IUGR. METHODS: We studied 22 group-housed baboons (ages 3-5 years). CTR (male n = 8, female n = 5) mothers ate ad libitum. IUGR (male n = 4, female n = 5) mothers were fed 70% feed eaten by CTR mothers during pregnancy and lactation. RESULTS: IUGR showed higher rates of aggressive displays (P < 0.01) and friendly displays (P < 0.02). Dominance ranks and physical aggression rates did not differ between groups. CONCLUSIONS: High rates of IUGR aggressive display might reflect developmental programming of behavioral phenotypes enhancing fitness. Friendly displays may reflect reconciliation. Potential mechanisms include neurodevelopment and learning. Exploration of IUGR as a risk factor for behavioral patterns is important for developing diagnostic and therapeutic strategies.

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

INTRODUCTION: Species 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. RESULTS: In 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. CONCLUSION: Cao 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.

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.

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.

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 (ßM) 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 ßM 24 hours apart at 0.6, 0.65, and 0.7 gestation. Offspring (saline control female, n = 7 and saline control male, n = 6; ßM female [FßM], n = 7 and ßM male [MßM], 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: ßM exposure decreased motivation in both sexes. In intra/extradimensional testing, FßM made more errors in the simple discrimination reversal (mean difference of errors [FßM - MßM] = 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 MßM 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 ßM exposures.

CANTAB delayed matching to sample task performance in juvenile baboons.

This study reports the administration of the Cambridge Neuropsychological Test Automated Battery system's 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.

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.

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.