Wild Gorillas Research Articles

Brain organization of gorillas reflects species differences in ecology.

Gorillas include separate eastern (Gorilla beringei) and western (Gorilla gorilla) African species that diverged from each other approximately 2 million years ago. Although anatomical, genetic, behavioral, and socioecological differences have been noted among gorilla populations, little is known about variation in their brain structure. This study examines neuroanatomical variation between gorilla species using structural neuroimaging. Postmortem magnetic resonance images were obtained of brains from 18 captive western lowland gorillas (Gorilla gorilla gorilla), 15 wild mountain gorillas (Gorilla beringei beringei), and 3 Grauer's gorillas (Gorilla beringei graueri) (both wild and captive). Stereologic methods were used to measure volumes of brain structures, including left and right frontal lobe gray and white matter, temporal lobe gray and white matter, parietal and occipital lobes gray and white matter, insular gray matter, hippocampus, striatum, thalamus, each hemisphere and the vermis of the cerebellum, and the external and extreme capsules together with the claustrum. Among the species differences, the volumes of the hippocampus and cerebellum were significantly larger in G. gorilla than G. beringei. These anatomical differences may relate to divergent ecological adaptations of the two species. Specifically, G. gorilla engages in more arboreal locomotion and thus may rely more on cerebellar circuits. In addition, they tend to eat more fruit and have larger home ranges and consequently might depend more on spatial mapping functions of the hippocampus.

Lactobacillus gorillae sp. nov., isolated from the faeces of captive and wild western lowland gorillas (Gorilla gorilla gorilla).

Four strains of Gram-staining-positive, anaerobic rods were isolated from the faeces of western lowland gorillas (Gorilla gorilla gorilla). Three strains, KZ01(T), KZ02 and KZ03, were isolated at the Kyoto City Zoo, Japan, and one strain, GG02, was isolated in the Moukalaba-Doudou National Park, Gabon. These strains were investigated taxonomically. These strains belonged to the Lactobacillus reuteri phylogenetic group according to phylogenetic analysis based on 16S rRNA gene sequences and specific phenotypic characteristics. Phylogenetic analysis of their 16S rRNA gene sequences revealed that strains KZ01(T), KZ02, KZ03 and GG02 formed a single monophyletic cluster and had a distinct line of descent. Based on sequence similarity of the 16S rRNA gene, Lactobacillus fermentum JCM 1173(T) (96.6 %) was the closest neighbour to these novel strains, although it was clear that these strains belonged to a different species. Partial pheS sequences also supported these relationships. DNA-DNA relatedness between strain KZ01(T) and L. fermentum JCM 1173(T) was less than 22 % and the DNA G+C content of strain KZ01(T) was 50.7 mol%. The cell-wall peptidoglycan type was A4β (l-Orn-d-Asp) and the major fatty acids were C16 : 0, C18 : 1ω9c and C19 : 1 cyclo 9,10. Therefore, based on phylogenetic, phenotypic and physiological evidence, these strains represent a novel species of the genus Lactobacillus, for which the name Lactobacillus gorillae sp. nov. is proposed. The type strain is KZ01(T) ( = JCM 19575(T) = DSM 28356(T)).

Pathogenic eukaryotes in gut microbiota of western lowland gorillas as revealed by molecular survey.

Although gorillas regarded as the largest extant species of primates and have a close phylogenetic relationship with humans, eukaryotic communities have not been previously studied in these populations. Herein, 35 eukaryotic primer sets targeting the 18S rRNA gene, internal transcribed spacer gene and other specific genes were used firstly to explore the eukaryotes in a fecal sample from a wild western lowland gorilla (Gorilla gorilla gorilla). Then specific real-time PCRs were achieved in additional 48 fecal samples from 21 individual gorillas to investigate the presence of human eukaryotic pathogens. In total, 1,572 clones were obtained and sequenced from the 15 cloning libraries, resulting in the retrieval of 87 eukaryotic species, including 52 fungi, 10 protozoa, 4 nematodes and 21 plant species, of which 52, 5, 2 and 21 species, respectively, have never before been described in gorillas. We also reported the occurrence of pathogenic fungi and parasites (i.e. Oesophagostomum bifurcum (86%), Necator americanus (43%), Candida tropicalis (81%) and other pathogenic fungi were identified). In conclusion, molecular techniques using multiple primer sets may offer an effective tool to study complex eukaryotic communities and to identify potential pathogens in the gastrointestinal tracts of primates.

Diversity of zoonotic enterohepatic Helicobacter species and detection of a putative novel gastric Helicobacter species in wild and wild-born captive chimpanzees and western lowland gorillas

A number of Helicobacter species cause gastrointestinal or hepatic disease in humans, including H. pylori, gastric non-H. pylori helicobacters from animal origin and enterohepatic Helicobacter species. Little is known on the presence of Helicobacter species in great apes, our closest living relatives and potential reservoirs of microorganisms that might emerge in humans. The aim of the present study was to investigate the presence of gastric and enterohepatic Helicobacter species in African chimpanzees and gorillas. Fresh fecal samples were collected from wild endangered chimpanzees and critically endangered western lowland gorillas from different African National Parks, as well as wild-born captive animals from primate sanctuaries. Intact Helicobacter bacteria were demonstrated in feces by fluorescence in situ hybridization. Screening using a Helicobacter genus-specific PCR revealed the presence of Helicobacter DNA in the majority of animals in all groups. Cloning and sequencing of 16S rRNA gene fragments revealed a high homology to sequences from various zoonotic enterohepatic Helicobacter species, including H. cinaedi and H. canadensis. A number of gorillas and chimpanzees also tested positive using PCR assays designed to amplify part of the ureAB gene cluster and the hsp60 gene of gastric helicobacters. Phylogenetic analysis revealed the presence of a putative novel zoonotic gastric Helicobacter taxon/species. For this species, we propose the name ‘Candidatus Helicobacter homininae’, pending isolation and further genetic characterization. The presence of several Helicobacter species not only implies a possible health threat for these endangered great apes, but also a possible zoonotic transmission of gastric and enterohepatic helicobacters from these primate reservoirs to humans.

Individual distinctiveness in call types of wild western female gorillas.

Individually distinct vocalizations play an important role in animal communication, allowing call recipients to respond differentially based on caller identity. However, which of the many calls in a species' repertoire should have more acoustic variability and be more recognizable is less apparent. One proposed hypothesis is that calls used over long distances should be more distinct because visual cues are not available to identify the caller. An alternative hypothesis proposes that close calls should be more recognizable because of their importance in social interactions. To examine which hypothesis garners more support, the acoustic variation and individual distinctiveness of eight call types of six wild western gorilla (Gorilla gorilla) females were investigated. Acoustic recordings of gorilla calls were collected at the Mondika Research Center (Republic of Congo). Acoustic variability was high in all gorilla calls. Similar high inter-individual variation and potential for identity coding (PIC) was found for all call types. Discriminant function analyses confirmed that all call types were individually distinct (although for call types with lowest sample size - hum, grumble and scream - this result cannot be generalized), suggesting that neither the distance at which communication occurs nor the call social function alone can explain the evolution of identity signaling in western gorilla communication.

Wild western lowland gorillas signal selectively using odor.

Mammals communicate socially through visual, auditory and chemical signals. The chemical sense is the oldest sense and is shared by all organisms including bacteria. Despite mounting evidence for social chemo-signaling in humans, the extent to which it modulates behavior is debated and can benefit from comparative models of closely related hominoids. The use of odor cues in wild ape social communication has been only rarely explored. Apart from one study on wild chimpanzee sniffing, our understanding is limited to anecdotes. We present the first study of wild gorilla chemo-communication and the first analysis of olfactory signaling in relation to arousal levels and odor strength in wild apes. If gorilla scent is used as a signaling mechanism instead of only a sign of arousal or stress, odor emission should be context specific and capable of variation as a function of the relationships between the emitter and perceiver(s). Measured through a human pungency scale, we determined the factors that predicted extreme levels of silverback odor for one wild western lowland gorilla (Gorilla gorilla gorilla) group silverback. Extreme silverback odor was predicted by the presence and intensity of inter-unit interactions, silverback anger, distress and long-calling auditory rates, and the absence of close proximity between the silverback and mother of the youngest infant. Odor strength also varied according to the focal silverback's strategic responses during high intensity inter-unit interactions. Silverbacks appear to use odor as a modifiable form of communication; where odor acts as a highly flexible, context dependent signaling mechanism to group members and extra-group units. The importance of olfaction to ape social communication may be especially pertinent in Central African forests where limited visibility may necessitate increased reliance on other senses.

Wild gorillas as a potential reservoir of Leishmania major.

Vector-borne parasites of the genus Leishmania are responsible for severe human diseases. Cutaneous leishmaniasis, a common form of the disease, is most often caused by the transmission of Leishmania major to humans by female phlebotomine sand flies. Apes are increasingly being seen as a source of zoonotic diseases, including malaria and rickettsiosis. To examine whether gorillas harbor Leishmania species, we screened fecal samples from wild western lowland gorillas (Gorilla gorilla gorilla) in Cameroon for the presence of these pathogens. Of 91 wild gorilla fecal samples, 12 contained Leishmania parasites, and 4 contained phlebotomine sand fly vectors. The molecular identity was determined by running 3 different polymerase chain reaction tests for detection of L. major. Next, fluorescence in situ hybridization was performed to visualize L. major parasites in fecal samples from the gorillas. Both promastigote and amastigote forms of the parasite were found. This work strongly suggests that wild gorillas carry pathogenic Leishmania parasites.

Vaccinating captive chimpanzees to save wild chimpanzees.

Infectious disease has only recently been recognized as a major threat to the survival of Endangered chimpanzees and Critically Endangered gorillas in the wild. One potentially powerful tool, vaccination, has not been deployed in fighting this disease threat, in good part because of fears about vaccine safety. Here we report on what is, to our knowledge, the first trial in which captive chimpanzees were used to test a vaccine intended for use on wild apes rather than humans. We tested a virus-like particle vaccine against Ebola virus, a leading source of death in wild gorillas and chimpanzees. The vaccine was safe and immunogenic. Captive trials of other vaccines and of methods for vaccine delivery hold great potential as weapons in the fight against wild ape extinction.

Twelve-year proximity relationships in a captive group of western lowland gorillas (Gorilla gorilla gorilla) at the San Diego Wild Animal Park, California, USA.

Proximity data were collected in a captive breeding group of gorillas (Gorilla gorilla gorilla) at the San Diego Wild Animal Park (currently called the San Diego Zoo Safari Park) twice a year (spring and fall periods) for over 12 years, by using a convenient method in which individuals less than 5 m from each animal in the group were recorded by scan sampling, approximately once per hour. Immature females from infancy to young adulthood maintained relatively frequent proximity to both their mothers and the silverback male and spent little time alone (no animals within 10 m), with relatively large individual differences. On the other hand, immature males decreased the time spent near their mothers and the silverback male and increased the time spent alone with increasing age. Therefore, sex differences in proximity to mothers and the silverback male became apparent after late juvenility. Some adult females maintained increased frequency of proximity to the silverback male than that by other females over the 12-year period, indicating the presence of long-term, stable proximity relationships between the silverback male and the adult females. Such long-term, stable proximity relationships were also observed among adult females. Some association patterns reported in wild gorillas, such as frequent proximity between adult females with dependent offspring and the silverback male and close relationships between related females, were not observed in the present study. The idiosyncratic or individual factors influencing some association patterns were easily reflected in captive situations.

Non-contiguous finished genome sequence and description of Paenibacillus gorillae sp. nov.

Strain G1T sp. nov. is the type strain of Paenibacillus gorillae a newly proposed species within the genus Paenibacillus. This strain, whose genome is described here, was isolated in France from the fecal sample of a wild western lowland gorilla from Cameroon. P. gorillae is a facultative anaerobic, Gram-negative, rod-shaped bacterium. Here we describe the features of this organism, together with the complete genome sequence and annotation. The 6,257,967 bp long genome (one chromosome but no plasmid) contains 5,856 protein-coding and 62 RNAs genes, including 60 tRNA genes.

Non-contiguous finished genome sequence and description of Gorillibacterium massiliense gen. nov, sp. nov., a new member of the family Paenibacillaceae.

Strain G5T gen. nov., sp. nov. is the type strain of Gorillibacterium massiliense, a newly proposed genus within the family Paenibacillaceae. This strain, whose genome is described here, was isolated in France from a stool sample of a wild Gorilla gorilla subsp. gorilla from Cameroon. G. massiliense is a facultatively anaerobic, Gram negative rod. Here we describe the features of this bacterium, together with the complete genome sequence and annotation. The 5,546,433 bp long genome (1 chromosome but no plasmid) contains 5,145 protein-coding and 76 RNA genes, including 69 tRNA genes.

Effects of habituation, research and ecotourism on faecal glucocorticoid metabolites in wild western lowland gorillas: Implications for conservation management

Wildlife tourism is proliferating worldwide and has the potential to raise revenue for conservation as well as public awareness of conservation issues. However, concerns are growing about the potentially negative influence of such tourism on the wildlife involved. We investigate the effects of habituation, ecotourism and research activities on levels of faecal glucocorticoid metabolites (FGCMs), a proxy for physiological stress, in wild western lowland gorillas (Gorilla gorilla gorilla) in the Central African Republic. We compare FGCMs in three human-contacted groups with those in unhabituated gorillas. We also explore how human–gorilla contact influences FGCMs of a gorilla group undergoing habituation and investigate how measures of general human–gorilla contact, tourism and human proximity influence FGCMs in recently and long-term habituated groups. Two of the three human-contacted groups had higher levels of FGCMs than unhabituated gorillas. The group undergoing habituation had the highest FGCMs, which increased up to 21days following contacts, suggesting a cumulative FGCM response, in line with descriptions of a hormonal adaptation response to a chronic intermittent stressor. FGCMs in habituated groups were significantly associated with increasing frequency of violation of the 7m distance rule by observers and with a medical intervention but not with other measures of human pressure. Our findings provide critical information for the management of this, and other, species whose conservation depends on habituation for ecotourism.

African origin of the malaria parasite Plasmodium vivax

Plasmodium vivax is the leading cause of human malaria in Asia and Latin America but is absent from most of central Africa due to the near fixation of a mutation that inhibits the expression of its receptor, the Duffy antigen, on human erythrocytes. The emergence of this protective allele is not understood because P. vivax is believed to have originated in Asia. Here we show, using a non-invasive approach, that wild chimpanzees and gorillas throughout central Africa are endemically infected with parasites that are closely related to human P. vivax. Sequence analyses reveal that ape parasites lack host specificity and are much more diverse than human parasites, which form a monophyletic lineage within the ape parasite radiation. These findings indicate that human P. vivax is of African origin and likely selected for the Duffy-negative mutation. All extant human P. vivax parasites are derived from a single ancestor that escaped out of Africa.

The Genome Sequence of Bifidobacterium moukalabense DSM 27321 Highlights the Close Phylogenetic Relatedness with the Bifidobacterium dentium Taxon

Bifidobacterium moukalabense DSM 27321 is the reference strain for a recently described new bifidobacterial species that has been isolated from a wild west lowland gorilla. Here, we report the whole-genome sequence of DSM 27321, which supports very close phylogenetic relatedness with members of the Bifidobacterium adolescentis phylogenetic group and, in particular, the Bifidobacterium dentium taxon.

Socioecological correlates of energy balance using urinary C-peptide measurements in wild female mountain gorillas

Maintaining a balanced energy budget is important for survival and reproduction, but measuring energy balance in wild animals has been fraught with difficulties. Female mountain gorillas are interesting subjects to examine environmental correlates of energy balance because their diet is primarily herbaceous vegetation, their food supply shows little seasonal variation and is abundant, yet they live in cooler, high-altitude habitats that may bring about energetic challenges. Social and reproductive parameters may also influence energy balance. Urinary C-peptide (UCP) has emerged as a valuable non-invasive biomarker of energy balance in primates. Here we use this method to investigate factors influencing energy balance in mountain gorillas of the Virunga Volcanoes, Rwanda. We examined a range of socioecological variables on energy balance in adult females in three groups monitored by the Karisoke Research Center over nine months. Three variables had significant effects on UCP levels: habitat (highest levels in the bamboo zone), season (highest levels in November during peak of the bamboo shoot availability) and day time (gradually increasing from early morning to early afternoon). There was no significant effect of reproductive state and dominance rank. Our study indicates that even in species that inhabit an area with a seemingly steady food supply, ecological variability can have pronounced effects on female energy balance.

A gorilla reservoir for human T-lymphotropic virus type 4

Of the seven known species of human retroviruses only one, human T-cell lymphotropic virus type 4 (HTLV-4), lacks a known animal reservoir. We report the largest screening for simian T-cell lymphotropic virus (STLV-4) to date in a wide range of captive and wild non-human primate (NHP) species from Cameroon. Among the 681 wild and 426 captive NHPs examined, we detected STLV-4 infection only among gorillas by using HTLV-4-specific quantitative polymerase chain reaction. The large number of samples analyzed, the diversity of NHP species examined, the geographic distribution of infected animals relative to the known HTLV-4 case, as well as detailed phylogenetic analyses on partial and full genomes, indicate that STLV-4 is endemic to gorillas, and that rather than being an ancient virus among humans, HTLV-4 emerged from a gorilla reservoir, likely through the hunting and butchering of wild gorillas. Our findings shed further light on the importance of gorillas as keystone reservoirs for the evolution and emergence of human infectious diseases and provide a clear course for preventing HTLV-4 emergence through management of human contact with wild gorillas, the development of improved assays for HTLV-4/STLV-4 detection and the ongoing monitoring of STLV-4 among gorillas and for HTLV-4 zoonosis among individuals exposed to gorilla populations.

RESPIRATORY DISEASE IN MOUNTAIN GORILLAS (GORILLA BERINGEI BERINGEI) IN RWANDA, 1990–2010: OUTBREAKS, CLINICAL COURSE, AND MEDICAL MANAGEMENT

Between 1990 and 2010, 18 outbreaks of respiratory disease occurred in Rwanda's wild human-habituated mountain gorillas (Gorilla beringei beringei). An outbreak was defined as clinically observable respiratory illness involving at least one third of all the gorillas in a family group (> 30% morbidity) over the course of at least 7 days. Outbreaks lasted 2 wk to 4 mo and affected up to five different gorilla family groups, either concurrently or sequentially. An outbreak was considered over if no further clinical illness was observed in the same or another group for at least 1 mo. Clinical signs varied from nasal discharge, sneezing, and mild intermittent coughing (mild), to spasmodic coughing, lethargy, and partial anorexia (moderate), to dyspnea, tachypnea, respiratory distress, weakness, complete anorexia, and occasionally death (severe). Nearly every mountain gorilla group habituated for tourism or research in Rwanda experienced at least one outbreak, and they may be increasing in frequency. In the first 15 yr of the review period 1990-2005, there were nine outbreaks involving 16 gorilla groups; in the last 5 yr of the review period, 2006-2010, there were nine outbreaks involving 11 groups. Although most gorillas recovered without treatment, 41 veterinary procedures were required to medically manage 35 severely ill individuals. Given the rise of mountain gorilla ecotourism in Rwanda, the possibility that respiratory disease results from contact with infected humans is of great concern, and both the etiology and epidemiology of this problem are active areas of research. The observed clinical signs, response to antimicrobial therapy among the sickest individuals, and postmortem findings are most consistent with viral upper respiratory tract infections complicated in some cases by secondary bacterial infections. The current gorilla visitation rules have been designed to minimize the risk of disease transmission between humans and wild human-habituated great apes.

Homme-gorilles et gorille-hommes : dynamiques de la frontière homme-animal et relations interethniques dans la forêt d’Afrique centrale

This paper (1) describes the perceptions of the western lowland gorilla (Gorilla gorilla gorilla) by forest dwellers of southeastern Cameroon and (2) investigates the sociocultural dimension of human–gorilla relationships focusing on folk theories of human–animal hybrids in which the gorilla is deeply embedded, enabling us to deal with the symbolic and social aspects of hunter-gatherer–farmer relations. The Baka hunter-gatherers of the southeast Cameroon–Congo border regions live with their Bakwele farming neighbors. They regard the Bakwele as gorilla–humans that may be reincarnated as gorillas after death. Conversely, the Bakwele regard the Baka as animal–humans that can transform themselves into various animals to raid crops, and believe that there are human–gorillas (dzil-elizaliza) in the wild gorilla population whose bodies are gorilla but whose spirits are those of human beings. There are two types of dzil-elizaliza: the revenant human-gorilla of the deceased, which is gentle and tranquil; and the witch-transformed human-gorilla, which is dangerous, malicious, and harms people. The dual nature of dzil-elizaliza expresses a contrast between the witch-controlled man-eater and the warm-hearted reincarnated ancestral relative in a human-gorilla. Ambivalent representations of dzil-elizaliza also seem to reflect variation of Bakwele’s self-image.Thus, Bakwele and gorillas can be said to share common properties which circulate across a human-nature landscape in the form of a human-animal hybrid. Local narratives of the human–gorilla demonstrate that gorillas are not only the subject of cultural construction that reflects specific people’s sociocultural conditions, but that they are also actors that sometimes intervene in actual social relationships. Here human and gorilla interactions are bidirectional. Much beyond food or symbols for humans, gorillas are human’s ontological counterparts. In this system, gorillas occupy a unique position that crosses both the interethnic boundaries between the Baka and the Bakwele and the interspecies boundaries between humans and animals. From the local people’s worldview, the maintenance of human and gorilla relationships is significant in their cultural practices and the separation of the two species is not desirable. This paper is a revised version of a book chapter published by Oishi, in Japanese in 2012.

Fatty acids in mountain gorilla diets: Implications for primate nutrition and health

Little is known about the fatty acid composition of foods eaten by wild primates. A total of 18 staple foods that comprise 97% of the annual dietary intake of the mountain gorilla (Gorilla beringei) were analyzed for fatty acid concentrations. Fruits and herbaceous leaves comprise the majority of the diet, with fruits generally having a higher mean percentage of fat (of dry matter; DM), as measured by ether extract (EE), than herbaceous leaves (13.0% ± SD 13.0% vs. 2.3 ± SD 0.8%). The mean daily EE intake by gorillas was 3.1% (DM). Fat provided ≈14% of the total dietary energy intake, and ≈22% of the dietary non-protein energy intake. Saturated fatty acids accounted for 32.4% of the total fatty acids in the diet, while monounsaturated fatty acids accounted for 12.5% and polyunsaturated fatty acids (PUFA) accounted for 54.6%. Both of the two essential PUFA, linoleic acid (LA, n-6) and α-linolenic acid (ALA, n-3), were found in all of the 17 staple foods containing crude fat and were among the three most predominant fatty acids in the diet: LA (C18:2n-6) (30.3%), palmitic acid (C16:0) (23.9%), and ALA (C18:3n-3) (21.2%). Herbaceous leaves had higher concentrations of ALA, while fruit was higher in LA. Fruits provided high amounts of fatty acids, especially LA, in proportion to their intake due to the higher fat concentrations; despite being low in fat, herbaceous leaves provided sufficient ALA due to the high intake of these foods. As expected, we found that wild mountain gorillas consume a diet lower in EE, than modern humans. The ratio of LA:ALA was 1.44, closer to agricultural paleolithic diets than to modern human diets.

Co-circulation of enteroviruses between apes and humans

A total of 139 stool samples from wild chimpanzees, gorillas and bonobos in Cameroon and Democratic Republic of Congo (DRC) were screened for enteroviruses (EVs) by reverse transcription PCR. Enterovirus RNA was detected in 10 % of samples, comprising eight from 58 sampled chimpanzees (13.8 %), one from 40 bonobos (2.5 %) and five from 40 gorillas (12.2 %). Three viruses isolated from chimpanzees grouped with human isolate EV-A89 and four (four chimpanzees, one gorilla) represented a newly identified type, EV-A119. These species A virus types overlapped with those circulating in human populations in the same area. The remaining six strains comprised a new species D type, EV-D120, infecting one chimpanzee and four gorillas, and a single EV variant infecting a bonobo that was remarkably divergent from other EVs and potentially constitutes a new enterovirus species. The study demonstrates both the circulation of genetically divergent EV variants in apes and monkeys as well as those shared with local human populations.