Gorilla Research Articles

Great ape walking kinematics: Implications for hominoid evolution.

Great apes provide a point of reference for understanding the evolution of locomotion in hominoids and early hominins. We assessed (1) the extent to which great apes use diagonal sequence, diagonal couplet gaits, like other primates, (2) the extent to which gait and posture vary across great apes, and (3) the role of body mass and limb proportions on ape quadrupedal kinematics. High-speed digital video of zoo-housed bonobos (Pan paniscus, N = 8), chimpanzees (Pan troglodytes, N = 13), lowland gorillas (Gorilla gorilla, N = 13), and orangutans (Pongo spp. N = 6) walking over-ground at self-selected speeds were used to determine the timing of limb touch-down, take-off, and to measure joint and segment angles at touch-down, midstance, and take-off. The great apes in our study showed broad kinematic and spatiotemporal similarity in quadrupedal walking. Size-adjusted walking speed was the strongest predictor of gait variables. Body mass had a negligible effect on variation in joint and segment angles, but stride frequency did trend higher among larger apes in analyses including size-adjusted speed. In contrast to most other primates, great apes did not favor diagonal sequence footfall patterns, but exhibited variable gait patterns that frequently shifted between diagonal and lateral sequences. Similarities in the terrestrial walking kinematics of extant great apes likely reflect their similar post-cranial anatomy and proportions. Our results suggest that the walking kinematics of orthograde, suspensory Miocene ape species were likely similar to living great apes, and highlight the utility of videographic and behavioral data in interpreting primate skeletal morphology.

Assessing the impact of seasonality on Cross River Gorilla Nest Construction at Kagwene Gorilla Sanctuary, North-West Cameroon

The Cross River gorilla, one of the most endangered subspecies of western gorilla (Gorilla gorilla) is endemic to 12 to 14 sites at the Cameroon-Nigeria border, where it is facing enormous threats from habitat loss, bush meat trade and minor climate changes (seasonal changes). In a strive to reduce the enormous stressors on this subspecies, this study assesses the impact of seasonality on nest construction by Cross River gorillas in the Kagwene Gorilla Sanctuary with the objective of evaluating the impact of seasonal changes on the nest construction. To achieve this goal, the study employed a hunter guided survey team, as well as guides/trackers of the Wildlife Conservation Society. This team regularly tracks and searches the forest for gorilla signs using vegetation trails, food prints, dung, and feeding signs which are subsequently followed onwards to the nesting site. Data were collected from January to December 2014. A total of 268 fresh gorilla nest sites were observed containing 1813 individual nests. Out of the 1813 nests recorded, 39.6% (N=718) of the nests were on the ground and 60.4% (N=1095) on trees. The frequency of each nest type varied significantly among months (P =0.4433). There was a significant effect of season on nest category. Ground categories (bare earth, herbaceous, woody and mixed) were more common in the dry season (74.9%) than in the wet season (25.1%). On the other hand, tree nests were more common in the wet season (77.4%) than in the dry season (22.6%). Mean nest diameter for the two seasons (dry and wet) was 1.1 and 1.3 m, respectively. The mean nest height was 12.5 m for both seasons. Cross River gorillas showed higher preferences for tree nests within the height class interval of 11 to 15 m (49.6%). The distribution of nests across gradient of altitudes did not vary significantly between seasons (P>0.05), and nests were most common on steep slopes (n=810). Seasonality did not significantly affect the choice of slope (P>0.05). There was a significant difference in the habitat types (primary forest, light gap, secondary forest and rock) used for nesting, with primary forest being most preferred. Nest site distribution was predominant in the northern section of the sanctuary. This study reveals that, both temperature and rainfall play an important role in nest construction by Cross River gorilla at Kagwene. Key words: Cross River gorilla, nest, seasonality, Kagwene Gorilla Sanctuary.

Body signals used during social play in captive immature western lowland gorillas.

The play face is a well-established play signal in nonhuman primates that functions to invite play and convey a playful intent. However, recent evidence indicates that some species display repertoires of play signals that may have more specific meanings related to particular aspects of play. Furthermore, previous studies have inconsistently categorized gorilla behaviors as play signals versus actual play. Here we aim to identify behaviors displayed by two immature captive western lowland gorillas (Gorilla gorilla gorilla) at the Buffalo Zoo that meet three necessary criteria to be considered play signals. Specifically, we (1) investigate whether 21 candidate signals are significantly different from actual play behaviors, (2) and from similar signals used in non-play contexts, and (3) determine whether they predict the occurrence of social play. The results indicate that at least 18 of the 21 candidate signals have strong support for classification as play signals. These findings represent first steps in determining the function of multiple play signals in gorillas.

Correction to: Do habituation, host traits and seasonality have an impact on protist and helminth infections of wild western lowland gorillas?

Affiliation of Klára J. Petrželková was incorrectly assigned as 2, 9, 10 in the original version of this article when in fact it should have been 3, 9, 10. Correct affiliations are presented here.

Impact of stress on the gut microbiome of free-ranging western lowland gorillas.

Exposure to stressors can negatively impact the mammalian gastrointestinal microbiome (GIM). Here, we used 454 pyrosequencing of 16S rRNA bacterial gene amplicons to evaluate the impact of physiological stress, as evidenced by faecal glucocorticoid metabolites (FGCM; ng/g), on the GIM composition of free-ranging western lowland gorillas (Gorilla gorilla gorilla). Although we found no relationship between GIM alpha diversity (H) and FGCM levels, we observed a significant relationship between the relative abundances of particular bacterial taxa and FGCM levels. Specifically, members of the family Anaerolineaceae (ρ=0.4, FDR q=0.01), genus Clostridium cluster XIVb (ρ=0.35, FDR q=0.02) and genus Oscillibacter (ρ=0.35, FDR q=0.02) were positively correlated with FGCM levels. Thus, while exposure to stressors appears to be associated with minor changes in the gorilla GIM, the consequences of these changes are unknown. Our results may have implications for conservation biology as well as for our overall understanding of factors influencing the non-human primate GIM.

Food cleaning in gorillas: Social learning is a possibility but not a necessity.

Food cleaning is widespread in the animal kingdom, and a recent report confirmed that (amongst other behaviours) wild western lowland gorillas also show food cleaning. The authors of this report conclude that this behaviour, based on its distribution patterns, constitutes a potential candidate for culture. While different conceptualisations of culture exist, some more and some less reliant on behavioural form copying, all of them assign a special role to social learning processes in explaining potentially cultural behaviours. Here we report the results of an experiment that tested to what extent food cleaning behaviour in a group of captive Western lowland gorillas (Gorilla gorilla gorilla) relies on social learning processes. Subjects were provided with clean and dirty apples. When they were provided with dirty apples, all subjects showed evidence of food cleaning in at least 75% of trials. Preferred cleaning techniques differed between individuals, four out of five of subjects expressed a behaviour analogous to that reported in wild conspecifics. Given this occurrence of food cleaning in a culturally unconnected population of gorillas, we conclude that social learning is unlikely to play a central role in the emergence of the food cleaning behavioural form in Western lowland gorillas; instead, placing a greater emphasis on individual learning of food cleaning’s behavioural form.

Great ape nutrition: low‐sugar and high‐fibre diets can lead to increased natural behaviours, decreased regurgitation and reingestion, and reversal of prediabetes

Great apes in captivity have been affected by a variety of conditions, including obesity, heart, gastrointestinal and dental diseases, and diabetes, all of which are at least influenced by an inappropriate diet. ‘Regurgitation and reingestion’ is also related to diet in great apes. Diets tend to be high in water‐soluble carbohydrates (WSC) (e.g. sugars and starches) and low in fibre. This study aimed to reduce the WSC and increase fibre concentrations of great ape diets, most notably for Chimpanzees Pan troglodytes, Bornean orangutans Pongo pygmaeus, Sumatran orangutans Pongo abelii and hybrid orangutans, and Western lowland gorillas Gorilla gorilla gorilla, and evaluate the behavioural and physiological responses of these species to the dietary changes. Wildlife Reserves Singapore had 4.8 Chimpanzees, 10.5 Bornean orangutans, 5.3 Sumatran orangutans and 2.1 P. pygmaeus × P. abelii orangutan hybrids, and Longleat Safari and Adventure Park, UK, had 4.0 Western lowland gorillas. Behaviour was recorded via scan sampling throughout the diet‐change process with a gradual decline in WSC. Five orangutans and two Chimpanzees were conditioned for finger pricking to monitor their blood‐glucose concentrations. The new diets led to changes in WSC from 59·0–64·3% to 47·5–47·7% and in neutral detergent fibre from 11·5–14·4% to 15·7–22·9% on a dry‐matter basis. These dietary changes significantly increased ‘travelling’, ‘foraging’ and ‘social affiliative’ behaviours, and decreased ‘inactivity’ and ‘abnormal behaviour patterns’, such as ‘regurgitation and reingestion’. Fasting blood glucose also decreased and, eventually, all great apes sampled had average blood‐glucose levels. Orangutans had a stronger insulin response compared with Chimpanzees, which may reflect their feeding ecology.

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

AbstractThe 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.

Do habituation, host traits and seasonality have an impact on protist and helminth infections of wild western lowland gorillas?

Increased anthropogenic activity can result in parasite exchanges and/or general changes in parasite communities, imposing a health risk to great apes. We studied protist and helminth parasites of wild western lowland gorilla groups in different levels of habituation, alongside humans inhabiting Dzanga-Sangha Protected Areas in the Central African Republic. Faeces were collected yearly during November and December from 2007 to 2010 and monthly from November 2010 to October 2011. Protist and helminth infections were compared among gorilla groups habituated, under habituation and unhabituated, and the effect of host traits and seasonality was evaluated. Zoonotic potential of parasites found in humans was assessed. No significant differences in clinically important parasites among the groups in different stages of habituation were found, except for Entamoeba spp. However, humans were infected with four taxa which may overlap with taxa found in gorillas. Females were less infected with spirurids, and adults had higher intensities of infection of Mammomonogamus sp. We found seasonal differences in the prevalence of several parasite taxa, but most importantly, the intensity of infection of unidentified strongylids was higher in the dry season. This study highlights that habituation may not necessarily pose a greater risk of protist and helminth infections in gorilla groups.

Morphometric, Behavioral, and Genomic Evidence for a New Orangutan Species

Six extant species of non-human great apes are currently recognized: Sumatran and Bornean orangutans, eastern and western gorillas, and chimpanzees and bonobos [1]. However, large gaps remain in our knowledge of fine-scale variation in hominoid morphology, behavior, and genetics, and aspects of great ape taxonomy remain in flux. This is particularly true for orangutans (genus: Pongo), the only Asian great apes and phylogenetically our most distant relatives among extant hominids [1]. Designation of Bornean and Sumatran orangutans, P.pygmaeus (Linnaeus 1760) and P.abelii (Lesson 1827), as distinct species occurred in 2001 [1, 2]. Here, we show that an isolated population from Batang Toru, at the southernmost range limit of extant Sumatran orangutans south of Lake Toba, is distinct from other northern Sumatran and Bornean populations. By comparing cranio-mandibular and dental characters of an orangutan killed in a human-animal conflict to those of 33 adult male orangutans of a similar developmental stage, we found consistent differences between the Batang Toru individual andother extant Ponginae. Our analyses of 37 orangutan genomes provided a second line of evidence. Model-based approaches revealed that the deepestsplit in the evolutionary history of extant orangutans occurred ∼3.38 mya between the Batang Toru population and those to the north of Lake Toba,whereas both currently recognized species separated much later, about 674 kya. Our combinedanalyses support a new classification of orangutans into three extant species. The new species, Pongo tapanuliensis, encompasses the Batang Toru population, of which fewer than 800 individuals survive. VIDEO ABSTRACT.

Using video and theater to increase knowledge and change attitudes-Why are gorillas important to the world and to Congo?

Applying environmental education in primate range countries is an important long-term activity to stimulate pro-conservation behavior. Within captive settings, mega-charismatic species, such as great apes are often used to increase knowledge and positively influence attitudes of visitors. Here, we evaluate the effectiveness of a short-term video and theater program developed for a Western audience and adapted to rural people living in two villages around Nouabalé-Ndoki National Park, Republic of Congo. We assessed the knowledge gain and attitude change using oral evaluation in the local language (N = 111). Overall pre-program knowledge about Western gorillas (Gorilla gorilla) was high. Detailed multivariate analysis of pre-program knowledge revealed differences in knowledge between two villages and people with different jobs while attitudes largely were similar between groups. The short-term education program was successful in raising knowledge, particularly of those people with less pre-program knowledge. We also noted an overall significant attitude improvement. Our data indicate short-term education programs are useful in quickly raising knowledge as well improving attitudes. Furthermore, education messages need to be clearly adapted to the daily livelihood realities of the audience, and multi-variate analysis can help to identify potential target groups for education programs.

Ambiguous Results When Using the Ambiguous-Cue Paradigm to Assess Learning and Cognitive Bias in Gorillas and a Black Bear.

Cognitive bias tests are frequently used to assess affective state in nonhumans. We adapted the ambiguous-cue paradigm to assess affective states and to compare learning of reward associations in two distantly related species, an American black bear and three Western lowland gorillas. Subjects were presented with three training stimuli: one that was always rewarded (P), one that was never rewarded (N) and one that was ambiguous (A) because its reward association depended on whether it had been paired with P (PA pairing) or N (NA pairing). Differential learning of NA and PA pairs provided insight into affective state as the bear and one gorilla learned NA pairs more readily, indicating that they focused on cues of reinforcement more than cues of non-reinforcement, whereas the opposite was true of one gorilla. A third gorilla did not learn either pairings at above chance levels. Although all subjects experienced difficulty learning the pairings, we were able to assess responses to A during probe trials in the bear and one gorilla. Both responded optimistically, but it was difficult to determine whether their responses were a true reflection of affective state or were due to preferences for specific stimuli.

A 3D musculoskeletal model of the western lowland gorilla hind limb: moment arms and torque of the hip, knee and ankle.

Three‐dimensional musculoskeletal models have become increasingly common for investigating muscle moment arms in studies of vertebrate locomotion. In this study we present the first musculoskeletal model of a western lowland gorilla hind limb. Moment arms of individual muscles around the hip, knee and ankle were compared with previously published data derived from the experimental tendon travel method. Considerable differences were found which we attribute to the different methodologies in this specific case. In this instance, we argue that our 3D model provides more accurate and reliable moment arm data than previously published data on the gorilla because our model incorporates more detailed consideration of the 3D geometry of muscles and the geometric constraints that exist on their lines‐of‐action about limb joints. Our new data have led us to revaluate the previous conclusion that muscle moment arms in the gorilla hind limb are optimised for locomotion with crouched or flexed limb postures. Furthermore, we found that bipedalism and terrestrial quadrupedalism coincided more regularly with higher moment arms and torque around the hip, knee and ankle than did vertical climbing. This indicates that the ability of a gorilla to walk bipedally is not restricted by musculoskeletal adaptations for quadrupedalism and vertical climbing, at least in terms of moment arms and torque about hind limb joints.

Watching the gorilla and questioning delivery dogma

Watching the gorilla and questioning delivery dogma

Gut microbiome composition is associated with cardiac disease in zoo-housed western lowland gorillas (Gorilla gorilla gorilla).

Cardiac disease is a leading cause of mortality in zoo-housed western lowland gorillas (Gorilla gorilla gorilla). The gut microbiome is associated with cardiac disease in humans and similarly the gut microbiome may be associated with cardiac diseases in close relatives of humans, such as gorillas. We assessed the relationship between cardiac disease and gut bacterial composition in eight zoo-housed male western lowland gorillas (N =4 with and N =4 without cardiac disease) utilizing 16S rRNA gene analysis on the Illumina MiSeq sequencing platform. We found bacterial composition differences between gorillas with and without cardiac disease. Bacterial operational taxonomic units from phyla Bacteroidetes, Spirochaetes, Proteobacteria and Firmicutes were significant indicators of cardiac disease. Our results suggest that further investigations between diet and cardiac disease could improve the management and health of zoo-housed populations of this endangered species.

Using demographic characteristics of populations to detect spatial fragmentation following suspected ebola outbreaks in great apes.

Demographic crashes due to emerging diseases can contribute to population fragmentation and increase extinction risk of small populations. Ebola outbreaks in 2002-2004 are suspected to have caused a decline of more than 80% in some Western lowland gorilla (Gorilla gorilla gorilla) populations. We investigated whether demographic indicators of this event allowed for the detection of spatial fragmentation in gorilla populations. We collected demographic data from two neighbouring populations: the Lokoué population, suspected to have been affected by an Ebola outbreak (followed from 2001 to 2014), and the Romani population, of unknown demographic status before Ebola outbreaks (followed from 2005 to 2014). Ten years after the outbreak, the Lokoué population is slowly recovering and the short-term demographic indicators of a population crash were no longer detectable. The Lokoué population has not experienced any additional demographic perturbation over the past decade. The Romani population did not show any of the demographic indicators of a population crash over the past decade. Its demographic structure remained similar to that of unaffected populations. Our results highlighted that the Ebola disease could contribute to fragmentation of gorilla populations due to the spatially heterogeneous impact of its outbreaks. The demographic structure of populations (i.e., age-sex and group structure) can be useful indicators of a possible occurrence of recent Ebola outbreaks in populations without known history, and may be more broadly used in other emerging disease/species systems. Longitudinal data are critical to our understanding of the impact of emerging diseases on wild populations and their conservation.

A RETROSPECTIVE REVIEW OF WESTERN LOWLAND GORILLA (GORILLA GORILLA GORILLA) MORTALITY IN EUROPEAN ZOOLOGIC COLLECTIONS BETWEEN 2004 AND 2014.

An understanding of the main causes of mortality among captive gorillas is imperative to promoting their optimal care, health, and welfare. A retrospective observational review of mortality among the European zoo-housed western lowland gorilla ( Gorilla gorilla gorilla) population from 2004 to 2014 was carried out. This is the first published study of mortality in this population. Relevant postmortem data were requested from each collection reporting a death during the study period. Age at death enabled grouping into discrete age categories. Deaths were classified according to cause. The main causes of death overall and for each age category and sex were identified. In total, 151 gorillas from 50 European collections died during the study period. Postmortem data were available for 119 (79%) of the deaths, of which 102 (86%) were classified by cause. Diseases of the digestive system were responsible for most (23%) deaths overall. Also of significance (each accounting for 15% overall mortality) were deaths due to external causes (especially trauma) among young gorillas and cardiovascular disease among adult and aged animals. Being a male gorilla was associated with an 8.77- and 5.40-fold increase in risk of death due to cardiovascular and respiratory disease, respectively. Death due to external causes was 4.45 times more likely among females than males. There was no statistically significant difference in life expectancy between male and female gorillas. The authors conclude that further work is needed to understand risk factors involved in the main causes of death and suggest a need for standardization with regard the approach to postmortem examination and data collection, sample collection, and storage across European zoos.

Identification and molecular characterization of novel primate bocaparvoviruses from wild western lowland gorillas of Moukalaba-Doudou National Park, Gabon

Bocaparvoviruses have been studied extensively owing to their ability to cause respiratory illness or gastroenteritis in humans. Some bocaparvoviruses have been detected in non-human primates (gorillas and chimpanzees), but the diversity and evolution of these viruses are not fully understood. In this study, we collected 107 fecal samples from wild western lowland gorillas in Moukalaba-Doudou National Park in Gabon to investigate the presence of bocaparvoviruses. Using a combination of pan-bocaparvovirus PCR and individual identification by microsatellite genotyping, we found that two samples from two apparently healthy infant gorillas were positive for bocaparvovirus. Sequencing and phylogenetic analyses revealed that the two gorilla bocaparvovirus strains are nearly identical and are closely related to viruses in the species Primate bocaparvovirus 2 (with 86.0% nucleotide identity to a human bocavirus 2 isolate). To our knowledge, this is the first report showing the presence of a non-human primate bocaparovirus within Primate bocaparvovirus 2. Our findings provide novel insights into the diversity and evolution of bocaparvoviruses and highlight the importance of surveying these viruses for the safe management of gorilla-based ecotourism.

Body growth and life history in wild mountain gorillas (Gorilla beringei beringei) from Volcanoes National Park, Rwanda.

Great apes show considerable diversity in socioecology and life history, but knowledge of their physical growth in natural settings is scarce. We characterized linear body size growth in wild mountain gorillas from Volcanoes National Park, Rwanda, a population distinguished by its extreme folivory and accelerated life histories. In 131 individuals (0.09-35.26 years), we used non-invasive parallel laser photogrammetry to measure body length, back width, arm length and two head dimensions. Nonparametric LOESS regression was used to characterize cross-sectional distance and velocity growth curves for males and females, and consider links with key life history milestones. Sex differences became evident between 8.5 and 10.0 years of age. Thereafter, female growth velocities declined, while males showed increased growth velocities until 10.0-14.5 years across dimensions. Body dimensions varied in growth; females and males reached 98% of maximum body length at 11.7 and 13.1 years, respectively. Females attained 95.3% of maximum body length by mean age at first birth. Neonates were 31% of maternal size, and doubled in size by mean weaning age. Males reached maximum body and arm length and back width before emigration, but experienced continued growth in head dimensions. While comparable data are scarce, our findings provide preliminary support for the prediction that mountain gorillas reach maximum body size at earlier ages compared to more frugivorous western gorillas. Data from other wild populations are needed to better understand comparative great ape development, and investigate links between trajectories of physical, behavioral, and reproductive maturation.

動物園飼育下のニシローランドゴリラの放飼場利用について(第7回日本生命倫理学会年次大会ワークショップ「動物への配慮と環境問題」発表原著)

動物園飼育下のニシローランドゴリラの放飼場利用について(第7回日本生命倫理学会年次大会ワークショップ「動物への配慮と環境問題」発表原著)