Gorilla Research Articles

Mosquitoes not bothered that humans smell different from apes

We have daubed ourselves with perfume for millennia, yet even when our aroma is concealed, blood-sucking pests still pinpoint juicy individuals. ‘We have studied why one person is more attractive to mosquitoes than another and we have shown that the odours produced by bacteria on the skin play an important role’, says Niels Verhulst, from the University of Zürich, Switzerland. But now Verhulst and colleagues from Wageningen University and Research, The Netherlands, and Zürich are turning their attention to the odours of some of our closest relatives: primates. As human populations are coming into increasing contact with wildlife displaced by habitat destruction – raising the risk that disease could skip from one species to another – Verhulst wondered how similar apes and humans smell from the perspective of disease-spreading mosquitoes.Verhulst swabbed the forearms of captive western lowland gorillas, bonobos, chimpanzees and ring-tailed lemurs in zoos across The Netherlands, as well as chimps in the Democratic Republic of Congo, to collect samples of the bacteria colonising the animals’ skins and their odours. In addition, he asked 15 male volunteers to avoid spicy food, alcohol, showering and hygiene products before collecting their skin odours and bacteria, while also collecting samples from local cows for comparison. Alexander Umanets then analysed the bacteria while Berhane Weldegergis investigated the individual components that comprised each animal's odour. Next, Jeroen Maas and Tessa Visser asked Anopheles coluzzi mosquitoes (which prefer to dine on humans) and Anopheles quadriannulatus (which have a preference for animals) which odour they preferred when offered the choice between human odour and one of the animal scents, to get a true sense of the odours’ similarities from the insect's perspective.Although the humans had the smallest variety of bacteria colonising their skin, their bacterial lodgers were more similar to those of the other primates than those of the cows. And when the team compared the animals’ scent cocktails, each was clearly unique, but the lemur's odour was more similar to that of the human volunteers; ‘something we did not expect’, says Verhulst. Comparing the mosquitoes’ preference for the human scent over cow odour, the team found that A. coluzzi were more partial to human odour, while A. quadriannulatus gravitated to the cow scent. However, the A. coluzzi mosquitoes were equally attracted to all of the primate odours, even ours, despite the differences between the primate and human scent cocktails.‘Apes do not smell like humans,’ says Verhulst, although he suggests that we may share some key odour components with our ape cousins, which could make us smell quite similar for mosquitoes.

Empirical selection between least-cost and current-flow designs for establishing wildlife corridors in Gabon.

Corridors are intended to increase species survival by abating landscape fragmentation resulting from the conversion of natural habitats into human-dominated matrices. Conservation scientists often rely on 1 type of corridor model, typically the least-cost model or current-flow model, to construct a linkage design, and their choice is not usually based on theory or empirical evidence. We developed a method to empirically confirm whether corridors produced by these 2 models are used by target species under current landscape conditions. We applied this method in the Gamba landscape between 2 national parks in southwestern Gabon. We collected signs of presence of African forest elephant (Loxodonta cyclotis), forest buffalo (Syncerus caffer nanus), and 2 apes, western lowland gorilla (Gorilla gorilla gorilla) and central chimpanzee (Pan troglodytes troglodytes), on transects. We used patch-occupancy models to identify least-cost and current-flow corridors for these 4 species. On average, 28.7% of current-flow corridors overlapped with least-cost corridors, confirming that the choice of corridor model can affect the location of the resulting linkage design. We validated these corridors by monitoring signs and examining camera detections on new transects within and outside modeled corridors. Current-flow corridors performed better than least-cost corridors for elephants, whereas the opposite was found for buffalo and apes. Locations of the highest priority corridors for the 3 taxa did not overlap, and only 18.3% of their combined surface was common among 2 species. We used centrality metrics to calculate the average contribution of corridor pixels to landscape connectivity and derived an index that can be used to prioritize corridors. As a result, we recommend protecting at least 17.4% of the land surface area around Gamba town to preserve the preferred travel routes of the target species.

In memorium: Koko, a remarkable gorilla.

In memorium: Koko, a remarkable gorilla.

Behavioral changes following alterations in the composition of a captive bachelor group of western lowland gorillas (Gorilla gorilla gorilla).

Western lowland gorillas (Gorilla gorilla gorilla) in zoos are housed in family or bachelor groups to maximize social opportunities. While wild bachelor groups are transient, all-male groups in zoos may be maintained for many years. Captive bachelor groups need to be carefully monitored, particularly during periods of demographic transition, due to the possibility for escalating aggression. We examined behavioral changes in a bachelor group at the Saint Louis Zoo following two significant alterations in group composition: (1) the introduction of two immature related males in 2011 and (2) the death of the dominant silverback in 2015. Behavioral data were collected on group members using 15 min focal observations with 30-s instantaneous scans, totaling 185.25 hr for the first transition and 115.25 hr for the second transition (with equal effort in baseline and transition periods). We found that the addition of the two subadult males resulted in a significant increase in affiliation in the group often initiated by these new younger individuals, while the rate of abnormal and aggressive behavior did not change significantly. The rate of abnormal, aggressive, or affiliative behavior in the group also did not change significantly following the death of the dominant silverback. Overall, we conclude that this bachelor group and potentially others can endure possibly destabilizing social transitions and remain cohesive social units. Behavioral changes will result from transitions, but the effect on individuals or impact on the group will vary. Therefore, longitudinal monitoring of bachelor groups will be essential for effective management during any major changes.

Noninvasive western lowland gorilla's health monitoring: A decade of simian immunodeficiency virus surveillance in southern Cameroon.

Simian immunodeficiency virus (SIVgor) causes persistent infection in critically endangered western lowland gorillas (Gorilla gorilla gorilla) from west central Africa. SIVgor is closely related to chimpanzee and human immunodeficiency viruses (SIVcpz and HIV‐1, respectively). We established a noninvasive method that does not interfere with gorillas' natural behaviour to provide wildlife pathogen surveillance and health monitoring for conservation. A total of 1,665 geo‐referenced fecal samples were collected at regular intervals from February 2006 to December 2014 (123 sampling days) in the Campo‐Ma'an National Park (southwest Cameroon). Host genotyping was performed using microsatellite markers, SIVgor infection was identified by serology and genetic amplification was attempted on seropositive individuals. We identified at least 125 distinct gorillas, 50 were resampled (observed 3.5 times in average) and 38 were SIVgor+ (seven individuals were seroconverters). Six groups of gorillas were identified based on the overlapping occurrence of individuals with apparent high rates of gene flow. We obtained SIVgor genetic sequences from 25 of 38 seropositive genotyped gorillas and showed that the virus follows exponential growth dynamics under a strict molecular clock. Different groups shared SIVgor lineages demonstrating intergroup viral spread and recapture of positive individuals illustrated intra‐host viral evolution. Relatedness and relationship genetic analysis of gorillas together with Bayesian phylogenetic inference of SIVgor provided evidence suggestive of vertical transmission. In conclusion, we provided insights into gorilla social dynamics and SIVgor evolution and emphasized the utility of noninvasive sampling to study wildlife health populations. These findings contribute to prospective planning for better monitoring and conservation.

Play signals, play moves: a gorilla critique of play theory

ABSTRACTPlay dates over a three-year study of two bachelor western lowland gorillas at the Philadelphia Zoo offer a critique of the idea of play as essentially a voluntary activity. Through video microanalysis, play emerges as negotiated interaction. The study goes beyond the primate ‘play face’ (PF) to understand the complexity of signaled play sessions and suggests that gorillas, like humans, have the equivalent of pregame ritual, and that play may climax cyclically, rather than begin with the PF. The study raises questions about the framing and coding of play behavior, play initiation, play signaling, and about the use of objects in social play.

Variation in the social organization of gorillas: Life history and socioecological perspectives.

A focus of socioecological research is to understand how ecological, social, and life history factors influence the variability of social organization within and between species. The genus Gorilla exhibits variability in social organization with western gorilla groups being almost exclusively one-male, yet approximately 40% of mountain gorilla groups are multimale. We review five ultimate causes for the variability in social organization within and among gorilla populations: human disturbance, ecological constraints on group size, risk of infanticide, life history patterns, and population density. We find the most evidence for the ecological constraints and life history hypotheses, but an over-riding explanation remains elusive. The variability may hinge on variation in female dispersal patterns, as females seek a group of optimal size and with a good protector male. Our review illustrates the challenges of understanding why the social organization of closely related species may deviate from predictions based on socioecological and life history theory.

Preliminary data showing potential for salivary C-reactive protein as an indicator of welfare in western lowland gorillas (Gorilla gorilla gorilla)

C-reactive protein (CRP) is an acute phase protein often used as a biomarker for inflammation related to acute trauma or chronic illness. Animal studies showing elevations in CRP following events such as road transport and moving to new housing suggest that CRP fluctuations may indicate how behavioral stress affects animal welfare. As part of a study about behavioral opportunities, salivary CRP was measured in three zoo-housed western lowland gorillas (Gorilla gorilla gorilla) to assess potential antiinflammatory effects of a foraging manipulation. Although the foraging conditions did not significantly affect CRP concentrations, an agonistic encounter—typical of the posturing that occurs among adolescent male gorillas—resulted in very minor injuries to one gorilla. Concentrations of salivary CRP increased over seventeen-fold for this gorilla, although his wounds were superficial and did not require veterinary treatment. Although animal care staff did not observe any wounds on the other two gorillas, CRP concentrations approximately doubled for both of them after this event, exceeding more than two standard deviations above their respective baselines. C-reactive protein was also correlated among individuals across the study period and with fecal glucocorticoid metabolite concentrations. These data provide first validation of CRP as a measure of the acute-phase response to injury in a gorilla and suggest that CRP may also fluctuate in response to social stressors, such as agonistic encounters. Salivary CRP may be a useful biomarker for several states that can contribute to negative welfare, including injury and social stress. These preliminary data should encourage additional investigations of CRP as a novel indicator of gorilla welfare.

Characteristics of Gorilla-Specific Lactobacillus Isolated from Captive and Wild Gorillas.

Lactic acid bacteria (LAB) reside in a wide range of mammals, such as autochthonous intestinal bacteria. In this paper, we present the phenotypic and phylogenetic characteristics of gorilla-specific LAB. Lactobacillus gorillae—previously isolated from the wild and captive western lowland gorillas (Gorilla gorilla gorilla)—were successfully isolated from wild mountain gorillas (Gorilla gorilla beringei) in addition to other captive and wild western lowland gorillas. The strains from wild gorillas could ferment D-xylose, arbutine, cellobiose, and trehalose better than those from captive gorillas. By contrast, tolerance to NaCl was higher in isolates from captive gorillas than in those from wild gorillas. This tendency may have been induced by regular foods in zoos, which contain sufficient amount of salts but less amount of indigestible fiber and plant secondary metabolites compared to foods in the wild. All strains of L. gorillae showed inhibitory activities to enteric pathogenic bacteria; however, the activity was significantly higher for strains from wild gorillas than for those from captive gorillas. This may have been induced by the captive condition with routine veterinary intervention. Since L. gorillae can grow in the gastrointestinal tract of gorillas in captivity, the strains from wild mountain gorillas are potential probiotics for gorillas under captive conditions.

Plasmodium ovale wallikeri in Western Lowland Gorillas and Humans, Central African Republic.

Human malaria parasites have rarely been reported from free-ranging great apes. Our study confirms the presence of the human malaria parasite Plasmodium ovale wallikeri in western lowland gorillas and humans in Dzanga Sangha Protected Areas, Central African Republic, and discusses implications for malaria epidemiology.

Visual Processing of Faces in Juvenile Western Lowland Gorillas without the Use of Training or Reinforcement: A Pilot Study

Visual Processing of Faces in Juvenile Western Lowland Gorillas without the Use of Training or Reinforcement: A Pilot Study

Anaerobic Fungi in Gorilla (Gorilla gorilla gorilla) Feces: an Adaptation to a High-Fiber Diet?

Many studies have demonstrated the importance of symbiotic microbial communities for the host with beneficial effects for nutrition, development, and the immune system. The majority of these studies have focused on bacteria residing in the gastrointestinal tract, while the fungal community has often been neglected. Gut anaerobic fungi of the class Neocallimastigomycetes are a vital part of the intestinal microbiome in many herbivorous animals and their exceptional abilities to degrade indigestible plant material means that they contribute significantly to fermentative processes in the enteric tract. Gorillas rely on a highly fibrous diet and depend on fermentative microorganisms to meet their daily energetic demands. To assess whether Neocallimastigomycetes occur in gorillas we analyzed 12 fecal samples from wild Western lowland gorillas (Gorilla gorilla gorilla) from Dzanga–Sangha Protected Areas, Central African Republic, and subjected potential anaerobic fungi sequences to phylogenetic analysis. The clone library contained ITS1 fragments that we related to 45 different fungi clones. Of these, 12 gastrointestinal fungi in gorillas are related to anaerobic fungi and our phylogenetic analyses support their assignment to the class Neocallimastigomycetes. As anaerobic fungi play a pivotal role in plant fiber degradation in the herbivore gut, gorillas might benefit from harboring these particular fungi with regard to their nutritional status. Future studies should investigate whether Neocallimastigomycetes are also found in other nonhuman primates with high fiber intake, which would also benefit from having such highly efficient fermentative microbes.

Validating the use of a commercial enzyme immunoassay to measure oxytocin in unextracted urine and saliva of the western lowland gorilla (Gorilla gorilla gorilla).

The neuroendocrine hormone oxytocin, which is an important physiological driver of social behavior and bonding, is increasingly being measured in conjunction with behavior to better understand primate sociality. To date no data are available on oxytocin concentrations within the genus Gorilla; however, as a result of their close genetic relatedness to humans, and tolerance-based social system, Gorilla represents an important group of study. The purpose of this study was to validate the measurement of urinary and salivary oxytocin in western lowland gorillas (Gorilla gorilla gorilla) to help facilitate future study of the interaction between oxytocin and behavior within the subspecies. The primary validation procedure was an intranasal challenge. Elevated oxytocin concentrations were observed in saliva samples taken 15-120min post challenge. Urine levels remained within baseline range approximately 30 and 90min following the challenge; however, elevated levels were observed 24h post challenge. No diurnal variation was found in salivary samples taken at regular intervals throughout the day; however, morning urine samples had higher concentrations than afternoon samples. In addition, samples were collected opportunistically following three social events: play, breeding, and the death of a conspecific. Following the play bouts, salivary oxytocin was almost three times greater than baseline. Salivary oxytocin was also significantly higher 15min post breeding compared to match-control samples. Following the death of a conspecific, the group mate's urinary oxytocin concentrations decreased by half compared to a baseline period when the group was intact. This study provides a biological validation of the measurement of urinary and salivary oxytocin in western lowland gorillas. These results suggest that urinary oxytocin measurements are suitable for establishing baseline levels, as they represent the build up of the previous day's concentrations, and salivary oxytocin measurements are suitable for assessing changes following specific events.

Long-term group membership and dynamics in a wild western lowland gorilla population (Gorilla gorilla gorilla) inferred using non-invasive genetics.

The social organization of a group-living animal is defined by a balance between group dynamic events such as group formation, group dissolution, and dispersal events and group stability in membership and over time. Understanding these processes, which are relevant for questions ranging from disease transmission patterns to the evolution of polygyny, requires long-term monitoring of multiple social units over time. Because all great ape species are long-lived and elusive, the number of studies on these key aspects of social organization are limited, especially for western lowland gorillas (Gorilla gorilla gorilla). In this study, we used non-invasive genetic samples collected within an approximately 100 km2 area of Loango National Park, Gabon to reconstruct group compositions and changes in composition over more than a decade. We identified 98 gorillas and 11 mixed sex groups sampled during 2014-2017. Using published data from 85 individuals and 12 groups surveyed between 2005 and 2009 at the same locality, we tracked groups and individuals back in time. The identification of 11 silverbacks via parentage analyses and the genetic tracking of 39 individuals across studies allowed us to infer six group formations, five group dissolutions, and 40 dispersal events within 12 years. We also observed four groups persisting across the sampling periods with a maximum inferred existence of nearly 17 years and exhibiting variation in membership stability. Our results highlight the variation in composition and stability among groups of western lowland gorillas and illustrate the power of non-invasive genetic sampling for long-term monitoring.

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.

‘Regurgitation and reingestion’ (R/R) in great apes: a review of current knowledge

Research indicates that regurgitation and reingestion (R/R) is a relatively common behaviour in zoo‐housed great apes, with most studies to date carried out on Western lowland gorillas Gorilla gorilla gorilla and Chimpanzees Pan troglodytes. R/R is an abnormal behaviour because great apes are not anatomically adapted to regurgitate their food as part of their normal feeding processes, and because this behaviour has not been observed in members of the species living freely in the wild, in conditions that would allow a full behavioural range. In this article, an overview is given of the published literature on R/R in great apes, which suggests that this behaviour is probably multifactorial and may be linked to inappropriate feeding environments (e.g. in terms of nutritional composition of the diet and/or presentation of food), and possibly also social and other factors. A similar behaviour to R/R, known as rumination disorder, can occur in humans (another great ape species), in whom it is classified as a feeding and eating disorder, and there are potential consequences to people's physical health as a result of oral acid. There have been no known studies to date to identify whether or not similar health consequences can occur in non‐human great apes, but the regurgitant has been found to be significantly more acidic in gorillas than the food they ingested originally, meaning it is potentially injurious in non‐human great apes. There is much that is not yet known about R/R and how to reduce or eliminate it when it does occur. The research indicates that there are a range of factors involved and these can vary by individual animal. More research into this behaviour is clearly needed to ensure that zoos and sanctuaries are providing the best possible care for these animals, and some suggestions for future research directions are included in this review.

Genetic and demographic analysis of European Endangered Species Programme (EEP) and Species Survival Plan (SSP) Western lowland gorilla Gorilla gorilla gorilla populations

Since the late 1990s, European Association of Zoos and Aquaria (EAZA)‐member zoos have worked collaboratively to achieve a self‐sustaining population for gorilla through the European Endangered Species Programme (EEP). The Association of Zoos and Aquariums (AZA) in the United States has similarly worked through the Species Survival Plan (SSP). These populations are all registered in the International Studbook for the Western Lowland Gorilla Gorilla g. gorilla Savage & Wyman, 1847, which is updated annually. Demographic and genetic analyses of these data are carried out to monitor population development. This paper presents the results of the genetic and demographic analysis of EAZA and AZA populations of the Western lowland gorilla Gorilla gorilla gorilla, considering the individuals registered since the beginning of the studbook (1950) until 2014, and the analyses are mainly focused on the results for both populations around the last decade. The data have been gathered from the 2014 international studbook and data registered in the Single Population Analysis and Records Keeping System (Sparks). Genetic and demographic analyses were carried out using PMx software. The results of the demographic analyses show that the EEP population is growing, demonstrating positive life parameters; for example, a finite growth rate of λ = 1·007, an instantaneous growth rate of r = 0·007 and a net reproductive rate of R0 = 1·160. However, the results of the demographic analyses for the SSP population show a general tendency for population reduction; that is, a finite growth rate of λ = 0·992, an instantaneous rate of growth rate r = −0·008 and a net reproductive rate of R0 = 0·864. When comparing the results from both populations it would appear that the application of strict breeding policies in the SSP for a few years had a noticeable impact on the SSP demographic results.

Global population records and managed‐programme updates for the great apes: short report

Keeping records of individual wild animals managed by zoos and aquariums is an essential component of population management, not only on the institutional scale but also to ensure long‐term health and viability of species populations regionally and globally. There are long‐established studbooks for Bornean orangutan Pongo pygmaeus, Sumatran orangutan Pongo abelii, Bonobo Pan paniscus, Chimpanzee Pan troglodytes sspp and Western lowland gorilla Gorilla gorilla gorilla. National and regional zoo and aquarium associations manage these population records through a variety of conservation programmes, ensuring the data are available for those working to conserve great apes and their habitats. This report presents updates for the great ape managed conservation programmes, with specific data provided for the 2016 global zoo populations.

Relationships Between Gastrointestinal Parasite Infections and the Fecal Microbiome in Free-Ranging Western Lowland Gorillas.

Relationships between gastrointestinal parasites (GIPs) and the gastrointestinal microbiome (GIM) are widely discussed topics across mammalian species due to their possible impact on the host's health. GIPs may change the environment determining alterations in GIM composition. We evaluated the associations between GIP infections and fecal microbiome composition in two habituated and two unhabituated groups of wild western lowland gorillas (Gorilla g. gorilla) from Dzanga Sangha Protected Areas, Central African Republic. We examined 43 fecal samples for GIPs and quantified strongylid nematodes. We characterized fecal microbiome composition through 454 pyrosequencing of the V1-V3 region of the bacterial 16S rRNA gene. Entamoeba spp. infections were associated with significant differences in abundances of bacterial taxa that likely play important roles in nutrition and metabolism for the host, besides being characteristic members of the gorilla gut microbiome. We did not observe any relationships between relative abundances of several bacterial taxa and strongylid egg counts. Based on our findings, we suggest that there is a significant relationship between fecal microbiome and Entamoeba infection in wild gorillas. This study contributes to the overall knowledge about factors involved in modulating GIM communities in great apes.

Gait characteristics of vertical climbing in mountain gorillas and chimpanzees

AbstractBiomechanical analyses of arboreal locomotion in great apes in their natural environment are scarce and thus attempts to correlate behavioral and habitat differences with variations in morphology are limited. The aim of this study was to investigate the gait characteristics of vertical climbing in mountain gorillas (Gorilla beringei beringei) and chimpanzees (Pan troglodytes) in a natural environment to assess differences in the climbing styles that may relate to variation in body size. We investigated temporal variables (i.e., cycle duration, duty factors, and stride frequency) and footfall sequences (i.e., diagonal vs. lateral sequence gaits) during vertical climbing (both ascent and descent) in 11 wild mountain gorillas and compared these data to those of eight semi‐free‐ranging chimpanzees, using video records ad libitum. Comparisons of temporal gait parameters revealed that large‐bodied mountain gorillas exhibited a longer cycle duration, lower stride frequency and generally a higher duty factor than small‐bodied chimpanzees. While both apes were similarly versatile in their vertical climbing performance in the natural environment, mountain gorillas most often engaged in diagonal sequence/diagonal couplet gaits and chimpanzees most often used lateral sequence/diagonal couplet gaits. This study revealed that mountain gorillas adapt their climbing strategy to accommodate their large body mass in a similar manner previously found in captive western lowland gorillas, and that chimpanzees are less variable in their climbing strategy than has been documented in captive bonobos.