Male genetic structure and paternity in western lowland gorillas (Gorilla gorilla gorilla)

The male dispersal patterns of western lowland gorillas (WLGs, Gorilla gorilla gorilla) are not well understood. To determine whether most silverbacks stay close to their relatives, we analyzed autosomal and Y‐chromosomal microsatellites (STRs) in wild WLGs at Moukalaba, Gabon. We obtained STR genotypes for 38 individuals, including eight silverbacks and 12 adult females in an approximately 40 km² area. Among them, 20 individuals were members of one identified group (Group Gentil; GG), including one silverback and six adult females. The silverback sired all 13 of the offspring in GG and no Y‐STR polymorphism within GG was found, as expected in a one‐male group structure. Over all silverbacks sampled, Y‐STR diversity was high considering the limited sampling area, and silverbacks with similar Y‐STR haplotypes were not always located in nearby areas. Although the misclassification rate of kinship estimates in this study was not negligible, there were no kin dyads among all silverbacks sampled. These results suggest that silverbacks born in the same group do not stay close to each other after maturation. The Y‐STR diversity in this study was similar to that of a previous study conducted in an area that was approximately 150 times larger than our study area. Similarity of WLG Y‐STR diversity between studies at different sampling scales suggests that male gene flow may not be geographically limited. These results suggest that WLG males normally disperse from their natal areas after maturation, at least, in Moukalaba. Am J Phys Anthropol 151:583–588, 2013. © 2013 Wiley Periodicals, Inc.     

Nutritional Aspects of Western Lowland Gorilla (Gorilla gorilla gorilla) Diet During Seasons of Fruit Scarcity at Bai Hokou,Central African Republic

Traditionally, gorillas were classified as folivores, yet 15 years of data on western lowland gorillas (Gorilla gorilla gorilla) show their diet to contain large quantities of foliage and fruit, and to vary both seasonally and annually. The consumption of fruit by gorillas at Bai Hokou, Central African Republic, is correlated with rainfall and ripe fruit availability (Remis, 1997a). We investigated the nutritional and chemical content of gorilla foods consumed at Bai Hokou during two seasons of fruit scarcity as measured by phenological observations and compared our findings with the nutrient content of gorilla foods at other African sites. We conclude that during lean times, Bai Hokou gorillas consumed fruits with higher levels of fiber and secondary compounds than those of other populations of western lowland or mountain gorillas. Conversely, leaves consumed by Bai Hokou gorillas were relatively low in fiber and tannins. Bai Hokou gorillas appeared to meet their nutritional needs by eating a combination of fruit and foliage. They ate fruits comparatively high in secondary compounds and fiber when necessary. While gorillas are selective feeders, wherever and whenever preferred foods are scarce, their large body size and digestive anatomy enable them to consume and process a broader repertoire of foods than smaller bodied-apes.     

Management of respiratory complications in a western lowland gorilla (Gorilla gorilla gorilla) born by cesarean section

A female western lowland gorilla (Gorilla gorilla gorilla) infant was delivered by cesarean section (C‐section) to an 18‐year‐old primiparous dam after prolonged labor. The infant required resuscitation at birth and was hospitalized for management of pneumonia and associated respiratory distress secondary to the aspiration of meconium‐stained amniotic fluid. The infant received nine days of intensive care with respiratory support, antibiotics, intravenous fluid therapy, anti‐inflammatory drugs, bronchodilators, and chest physiotherapy. Respiratory support included nasal continuous positive airway pressure (CPAP), and supplemental oxygen. Complications included right lung atelectasis secondary to bronchial obstruction and pneumonia. Following the resolution of pneumonia, visual reintroductions with the troop were initiated. The dam was given a medical lactation supplement (metoclopramide) and her mammary glands were stimulated to increase milk production. After several days of visual and olfactory introductions, the infant was successfully physically reintroduced to her dam at 12 days of age; the dam showed appropriate maternal response and nursing of the infant. The infant had appropriate growth and development, and 4 years later, has no evidence of negative side effects of neonatal respiratory disease. This is the first reported case of management of neonatal gorilla respiratory disease associated with a C‐section, with successful reintroduction to the family group after hospitalization.     

Nutritional geometry: gorillas prioritize non-protein energy while consuming surplus protein

It is widely assumed that terrestrial food webs are built on a nitrogen-limited base and consequently herbivores must compensate through selection of high-protein foods and efficient nitrogen retention. Like many folivorous primates, gorillas' diet selection supports this assumption, as they apparently prefer protein-rich foods. Our study of mountain gorillas (Gorilla beringei) in Uganda revealed that, in some periods, carbohydrate-rich fruits displace a large portion of protein-rich leaves in their diet. We show that non-protein energy (NPE) intake was invariant throughout the year, whereas protein intake was substantially higher when leaves were the major portion of the diet. This pattern of macronutrient intake suggests that gorillas prioritize NPE and, to achieve this when leaves are the major dietary item, they over-eat protein. The concentrations of protein consumed in relation to energy when leaves were the major portion of the diet were close to the maximum recommended for humans and similar to high-protein human weight-loss diets. By contrast, the concentrations of protein in relation to energy when gorillas ate fruit-dominated diets were similar to those recommended for humans. Our results question the generality of nitrogen limitation in terrestrial herbivores and provide a fascinating contrast with human macronutrient intake.     

Metastatic endocervical adenocarcinoma in a western lowland gorilla (Gorilla g. gorilla): no evidence of virus-induced carcinogenesis

Background Cervical Cancer is the second most common cancer among women. Nevertheless, similar tumours have only been rarely described in Great Apes. This report characterizes the pathological and molecular features of a metastatic endocervical adenocarcinoma in a Western lowland gorilla (Gorilla g. gorilla). Methods Necropsy and histopathology was performed to identify the cause of the disease in an cachectic 50‐year‐old western lowland gorilla. Immunohistochemistry for Ki67, oestrogen receptor alpha and ERBB2 was performed to characterize the tumor. In addition, Pan‐herpesvirus and Pan‐papillomavirus PCR were used to identify a possible viral cause. Results The endoccervical carcinoma showed a severe metastatic spread to the lung, brain and bone and was herpesvirus and papillomavirus‐negative. Most tumor cells were ERBB2‐positive, 15% of tumor cells were Ki67‐positive and only few tumor cells had oestrogen receptor alpha expression. Conclusions Histopathologically and immunohistochemically, the tumour had striking similarities to human endocervicial adenocarcinomas of the common type. However, PCR analysis failed to identify herpes‐ or papillomaviral DNA in the tumor at the time of necropsy, thus leaving the question for cause of the disease open.     

Gut microbiome composition and metabolomic profiles of wild western lowland gorillas (Gorilla gorilla gorilla) reflect host ecology

The metabolic activities of gut microbes significantly influence host physiology; thus, characterizing the forces that modulate this micro‐ecosystem is key to understanding mammalian biology and fitness. To investigate the gut microbiome of wild primates and determine how these microbial communities respond to the host's external environment, we characterized faecal bacterial communities and, for the first time, gut metabolomes of four wild lowland gorilla groups in the Dzanga‐Sangha Protected Areas, Central African Republic. Results show that geographical range may be an important modulator of the gut microbiomes and metabolomes of these gorilla groups. Distinctions seemed to relate to feeding behaviour, implying energy harvest through increased fruit consumption or fermentation of highly fibrous foods. These observations were supported by differential abundance of metabolites and bacterial taxa associated with the metabolism of cellulose, phenolics, organic acids, simple sugars, lipids and sterols between gorillas occupying different geographical ranges. Additionally, the gut microbiomes of a gorilla group under increased anthropogenic pressure could always be distinguished from that of all other groups. By characterizing the interplay between environment, behaviour, diet and symbiotic gut microbes, we present an alternative perspective on primate ecology and on the forces that shape the gut microbiomes of wild primates from an evolutionary context.     

Proximate composition of milk from free-ranging mountain gorillas (Gorilla beringei beringei)

Published data on milk composition for nonhuman primates, especially great apes, are lacking. Milk composition data are important for understanding the physiology and evolution of mammalian milk production, as well as the nutritional requirements of infants. For many primate species these data have added relevance because of the need to hand raise infants orphaned by poaching or separated from their mothers in captivity. The proximate composition (dry matter (DM), protein, fat, sugar) of free-ranging mountain gorilla (MG) (Gorilla beringei beringei) milk was characterized from samples (N = 10) collected opportunistically during field procedures. The mean values for mid-lactation (1-50 months) milk samples from healthy MGs (N = 7) were: 10.7% DM, 1.9% fat, 1.4% crude protein, 6.8% sugar, and 0.53 kcal/g. These results are lower in fat and total energy than most other Hominidae, including humans. One early-lactation sample was high in protein content while the composition of two samples from gorillas with poor health and suspected poor milk quality both deviated from the normal, mid-lactation pattern. This survey adds to the data available for primate milk composition and suggests that wild MG infants normally consume milk that is lower in fat and total energy than human milk.     

The function of loud calls (Hoot Series) in wild western gorillas (Gorilla gorilla)

The use of loud vocal signals to reduce distance among separated social partners is well documented in many species; however, the underlying mechanisms by which the reduction of spacing occurs and how they differ across species remain unclear. Western gorillas (Gorilla gorilla) offer an opportunity to investigate these issues because their vocal repertoire includes a loud, long‐distance call (i.e., hoot series) that is potentially used in within‐group communication, whereas mountain gorillas use an identical call exclusively during intergroup encounters. First, we tested whether the hoot series functions as a contact/separation call. Second, we examined which individuals were more likely to reply and which party was more responsible for decreasing distance to identify the underlying mechanisms and cognitive implications of hoot series. We collected behavioral, spatial, and acoustic data on five adult gorillas over 15 months at the Mondika Research Center (Republic of Congo and CAR). Hoot series are individually distinct calls and given by both male and female gorillas when separated from each other. Following hooting, the distance between separated group members decreased significantly; thus we concluded that western gorillas use this call to reestablish group cohesion. The way in which proximity was achieved depended upon listeners replying or not to the caller. Replies may indicate a conflict between callers about intended travel direction, with vocal interchanges serving to negotiate a consensus. Although the acoustic features of vocal signals are highly constrained in closely related species, our results demonstrate that the function and usage of particular calls can be flexible. Am J Phys Anthropol 155:379–391, 2014. © 2014 Wiley Periodicals, Inc.     

The development of infant play in a captive group of lowland gorillas (Gorilla gorilla gorilla)

Three infant gorillas born at the Yerkes Regional Primate Research Center of Emory University were studied during their first year and one-half of life for various aspects of behavior, including solitary and social play, using both focal animal and one-zero sampling. The appearance of play in these infants followed a developmental trend, beginning with mother-infant play, and followed by solitary play, and then social play among peers. Mothers were initially very vigilant, repeatedly interrupting infant peer play bouts, this relaxing toward the end of the first year. Evidence for a possible sex difference in active social play is presented.     

Wild Bornean orangutan (Pongo pygmaeus wurmbii) feeding rates and the Marginal Value Theorem

The Marginal Value Theorem (MVT) is an integral supplement to Optimal Foraging Theory (OFT) as it seeks to explain an animal's decision of when to leave a patch when food is still available. MVT predicts that a forager capable of depleting a patch, in a habitat where food is patchily distributed, will leave the patch when the intake rate within it decreases to the average intake rate for the habitat. MVT relies on the critical assumption that the feeding rate in the patch will decrease over time. We tested this assumption using feeding data from a population of wild Bornean orangutans (Pongo pygmaeus wurmbii) from Gunung Palung National Park. We hypothesized that the feeding rate within orangutan food patches would decrease over time. Data included feeding bouts from continuous focal follows between 2014 and 2016. We recorded the average feeding rate over each tertile of the bout, as well as the first, midpoint, and last feeding rates collected. We did not find evidence of a decrease between first and last feeding rates (Linear Mixed Effects Model, n = 63), between a mid-point and last rate (Linear Mixed Effects Model, n = 63), between the tertiles (Linear Mixed Effects Model, n = 63), nor a decrease in feeding rate overall (Linear Mixed Effects Model, n = 146). These findings, thus, do not support the MVT assumption of decreased patch feeding rates over time in this large generalist frugivore.     

Sex-biased dispersal in western lowland gorillas (Gorilla gorilla gorilla)

We explored two hypotheses related to potential differences between sexes in dispersal behaviour in western lowland gorillas (Gorilla gorilla gorilla). Direct observations suggest that immature females have more opportunities to move between breeding groups than immature males. The distribution of kin dyadic relationships within and between groups does not, however, support this hypothesis. At larger geographical scales, dispersal is likely to be easier for males than females because of the solitary phase most blackbacks experience before founding their own breeding group. However, previous work indicates that males settle preferentially close to male kin. By specifically tracing female and male lineages with mitochondrial and Y-chromosomal genetic markers, we found that male gorillas in the 6000 km2 area we surveyed form a single population whereas females are restricted to the individual sites we sampled and do not freely move around this area. These differences are more correctly described as differences in dispersal distances, rather than differences in dispersal rates between sexes (both sexes emigrate from their natal group in this species). Differences in resource competition and dispersal costs between female and male gorillas are compatible with the observed pattern, but more work is needed to understand if these ultimate causes are responsible for sex-biased dispersal distances in western lowland gorillas.     

Fatal ulcerative colitis in a western lowland gorilla (Gorilla gorilla gorilla)

A captive western lowland gorilla (Gorilla gorilla gorilla) presented with watery diarrhoea that progressed to become profuse and haemorrhagic. Faecal analyses revealed Balantidium (B.) coli trophozoites and salmonella-like bacteria. Despite treatment the gorilla died on the 5th day after onset of symptoms. Post-mortem examination revealed a severe erosive-ulcerative superficial and deep colitis. Histological examination of post-mortem samples of the colon showed plentiful B. coli invading into the mucosa and submucosa, whilst PCR screening of bacterial DNA could not confirm any bacteria species which could be connected to the clinical picture. As B. coli is usually a non-pathogenic gut commensal, and as this animal previously showed evidence of non-symptomatic infection of B. coli, it is possible that the switch in pathogenicity was triggered by an acute bacterial infection. Despite successful treatment of the bacterial infection the secondary deep invasion of B. coli was not reversed, possibly because of the failure of the treatment regimen, and led to the death of the gorilla.     

Brain structure variation in great apes, with attention to the mountain gorilla (Gorilla beringei beringei)

This report presents data regarding the brain structure of mountain gorillas (Gorilla beringei beringei) in comparison with other great apes. Magnetic resonance (MR) images of three mountain gorilla brains were obtained with a 3T scanner, and the volume of major neuroanatomical structures (neocortical gray matter, hippocampus, thalamus, striatum, and cerebellum) was measured. These data were included with our existing database that includes 23 chimpanzees, three western lowland gorillas, and six orangutans. We defined a multidimensional space by calculating the principal components (PCs) from the correlation matrix of brain structure fractions in the well-represented sample of chimpanzees. We then plotted data from all of the taxa in this space to examine phyletic variation in neural organization. Most of the variance in mountain gorillas, as well as other great apes, was contained within the chimpanzee range along the first two PCs, which accounted for 61.73% of the total variance. Thus, the majority of interspecific variation in brain structure observed among these ape taxa was no greater than the within-species variation seen in chimpanzees. The loadings on PCs indicated that the brain structure of great apes differs among taxa mostly in the relative sizes of the striatum, cerebellum, and hippocampus. These findings suggest possible functional differences among taxa in terms of neural adaptations for ecological and locomotor capacities. Importantly, these results fill a critical gap in current knowledge regarding great ape neuroanatomical diversity.     

Seed dispersal effectiveness of the western lowland gorilla (Gorilla gorilla gorilla) in Gabon

The quantitative and qualitative aspects of seed dispersal by the western lowland gorilla (Gorilla gorilla gorilla) were investigated in Gabon. Fresh faeces were collected and washed to identify and count the seeds. Seed germinability after gut passage was estimated with trials in a nursery at the study site. To assess the impact of gut passage on germination success and delay, comparative trials were run with four treatments: (i) gut passed seeds cleaned of faeces, (ii) gut passed seeds within a faecal matrix, (iii) seeds from fresh fruits surrounded by pulp, and (iv) seeds from fresh fruits cleaned of pulp. The analysis of 180 faecal units resulted in the identification of 58 species of seed. Germination trials were realized for 55 species and the mean germination success reached 46%. The impact of gut passage was investigated for Santiria trimera and Chrysophyllum lacourtianum; both species displayed higher germination success after ingestion. This study shows that gorillas effectively disperse seeds of numerous plant species, many of which provide timber or nontimber forest products or are typical of Gabonese forests. Considering the high‐quality of gorilla deposition sites, gorillas is thought to play a unique role in the dynamics of Central African forest.