Wild Gorillas Research Articles

Bifidobacterium moukalabense sp. nov., isolated from the faeces of wild west lowland gorilla (Gorilla gorilla gorilla)

Gram-staining-positive anaerobic rods were isolated from the faeces of a wild lowland gorilla (Gorilla gorilla gorilla) in Moukalaba-Doudou National Park, Gabon, and strain GG01(T) was taxonomically investigated. Based on phylogenetic analyses and specific phenotypic characteristics, the strain belonged to the genus Bifidobacterium. Phylogenetic analysis of its 16S rRNA gene sequence revealed that strain GG01(T) formed a single monophyletic cluster and had a distinct line of descent. Based on 16S rRNA gene sequence similarity, the type strains of Bifidobacterium catenulatum JCM 1194(T) (98.3%) and Bifidobacterium pseudocatenulatum (98.1%) JCM 1200(T) were the most closely related to this novel strain, although it was clear that they belonged to different species. hsp60 sequences also supported these relationships. The DNA G+C content of this novel strain was 60.1 mol%. Bifidobacterium moukalabense sp. nov. (type strain GG01(T) = JCM 18751(T) = DSM 27321(T)) is proposed.

Possible tool use in a mountain gorilla

Here we report a description of putative tool use in wild mountain gorillas. At the Dian Fossey Gorilla Fund's Karisoke Research Center in Volcanoes National Park (Rwanda), an adult female was observed using a bamboo culm as a ladder for her offspring. This is one of only a few documented cases of possible tool use in wild gorillas, although tool use behavior is commonly observed in captive gorillas. Although the behavior observed may have been incidental, the present report in combination with previous evidence (Breuer et al., 2005) suggests that tool use in gorillas occurs outside the context of food acquisition and may be directed at overcoming physical obstacles in complex rugged microhabitats such as bamboo forest and swamps.

Non-contiguous finished genome sequence and description of Bacillus massiliogorillae sp. nov.

Strain G2T sp. nov. is the type strain of B. massiliogorillae, a proposed new species within the genus Bacillus. This strain, whose genome is described here, was isolated in France from the fecal sample of a wild western lowland gorilla from Cameroon. B. massiliogorillae is a facultative anaerobic, Gram-variable, rod-shaped bacterium. Here we describe the features of this organism, together with the complete genome sequence and annotation. The 5,431,633 bp long genome (1 chromosome but no plasmid) contains 5,179 protein-coding and 98 RNA genes, including 91 tRNA genes.

Monitoring ovarian cycle activity via progestagens in urine and feces of female mountain gorillas: A comparison of EIA and LC–MS measurements

Understanding the reproductive biology of endangered mountain gorillas (Gorilla beringei beringei) is essential for optimizing conservation strategies, determining any demographic impact of socioecological changes, and providing information for comparative studies of primates. Non-invasive techniques have been used to assess the reproductive function of many primates and the importance of validating the measurements of hormones metabolites is widely recognized because they may vary even within closely related species. To determine if it is possible to non-invasively monitor ovarian activity in wild mountain gorillas, we used enzyme immunoassays (EIA) to quantify both urinary and fecal excretion of immunoreactive pregnanediol-3-glucuronide (iPdG), defined as all metabolites detected by a pregnanediol-3-glucuronide immunoassay (PdG EIA). Simultaneously, we performed the liquid chromatography mass spectrometry (LC-MS) to quantify the excretion of pregnanediol in urine and feces. Samples were analyzed over nine cycles of five females from the habituated gorillas monitored by Karisoke Research Center, Rwanda. As an additional indicator for ovulation timing, estrone conjugates (E1C) were measured in a subset of urine samples. The concentrations of iPdG and pregnanediol measured in the same samples were significantly correlated. Urinary concentrations of iPdG and pregnanediol fluctuated over the menstrual cycle but did not reveal any cyclic pattern, whereas a typical preovulatory urinary E1C surge and postovulatory increases of fecal iPdG and pregnanediol were detected. The luteal peaks of iPdG and pregnanediol levels in feces were on average 2.8 and 7.6 times higher, respectively, than averaged levels in the corresponding follicular phase. The relative number of days with observed matings was higher within the presumed fertile window than in the preceding period. Overall, the results indicate that fecal analysis of iPdG and pregnanediol is suitable for detecting ovulation in female mountain gorillas. Urinary measurements using both EIA and LC-MS appeared to be uninformative for monitoring ovarian activity in this primate.

Variability in the developmental life history of the genusGorilla

Life history is influenced by factors both intrinsic (e.g., body and relative brain size) and extrinsic (e.g., diet, environmental instability) to organisms. In this study, we examine the prediction that energetic risk influences the life history of gorillas. Recent comparisons suggest that the more frugivorous western lowland gorilla shows increased infant dependence, and thus a slower life history, than the primarily folivorous mountain gorilla to buffer against the risk of starvation during periods of food unpredictability. We further tested this hypothesis by incorporating additional life history data from wild western lowland gorillas and captive western lowland gorillas with the assumption that the latter live under ecological conditions of energetic risk that more closely resemble those of mountain gorillas and thus should show faster life histories than wild members of the species. Overall, we found captive western lowland and wild mountain gorillas to have faster developmental life histories than wild western lowland gorillas, weaning their infants approximately a year earlier and thus reducing interbirth intervals by a year. These results provide support that energetic risk plays an important role in determining gorilla life history. Unlike previous assertions, gorillas do not have substantially faster life histories, at least at the genus level, than other great apes. This calls for a re-evaluation of theories concerning comparative ape life history and evolution and highlights the need for data from additional populations that vary in energetic risk.

Western Gorilla Vocal Repertoire and Contextual Use of Vocalizations

AbstractDespite considerable interest in the vocal communication of non‐human primates and its possible relevance to theories of language evolution, we know surprisingly little about how vocal communication varies between closely related species inhabiting differing environments. Here, we provide the first quantitative description of the vocal repertoire, calling rates, and call usage in wild western gorillas and compare it to the previous work on mountain gorilla vocal behavior. During 1572 h of focal follows (n = 533), we collected behavioral data on and recorded vocalizations (n = 2163) of eight individuals in one group atMondikaResearchCenter (Republic ofCongo). We supplemented these data with opportunistic recordings of an additional adult male in a second group. We used discriminant function analysis to test how well calls can be categorized by their acoustic structure and used behavioral data to determine the typical usage of western gorilla call types. The vocal repertoire comprised of 17 call types. Twelve of 17 call types were given primarily in a single context. Our results were similar to previous studies of mountain gorillas in that grunts, and grumbles were used most frequently and the silverback male vocalized more frequently than other group members. However, compared to mountain gorillas, western gorillas used an additional call type (sex‐whinny), used a second call type (hoot series) in a completely different context and by all age–sex classes, and used many more call types in a more context‐specific fashion. Our study suggests that although vocal production is highly constrained by morphology and phylogeny, differing social and ecological conditions can yield differences in the use and function of calls, even between two closely related species such as western and mountain gorillas.

Adenoviruses isolated from wild gorillas are closely related to human species C viruses

We have isolated and cultured three distinct adenoviruses from wild gorillas. Phylogenetic analysis grouped the viruses with human adenovirus species C based on DNA polymerase, hexon, and E4ORF6 genes. The three wild gorilla adenoviruses clustered with the other species C captive gorilla adenoviruses, forming a branch separate from human and chimpanzee/bonobo adenoviruses. Animal sera to the three newly isolated viruses did not cross-neutralize, demonstrating serological distinctiveness. The human adenovirus 5 fiber knob blocked infection, suggesting use of the Coxsackie and Adenovirus Receptor. These viruses may provide viral vectors with properties distinct from chimpanzee adenovirus and human adenovirus vectors.

A Genome-Wide Survey of Genetic Variation in Gorillas Using Reduced Representation Sequencing

All non-human great apes are endangered in the wild, and it is therefore important to gain an understanding of their demography and genetic diversity. Whole genome assembly projects have provided an invaluable foundation for understanding genetics in all four genera, but to date genetic studies of multiple individuals within great ape species have largely been confined to mitochondrial DNA and a small number of other loci. Here, we present a genome-wide survey of genetic variation in gorillas using a reduced representation sequencing approach, focusing on the two lowland subspecies. We identify 3,006,670 polymorphic sites in 14 individuals: 12 western lowland gorillas (Gorilla gorilla gorilla) and 2 eastern lowland gorillas (Gorilla beringei graueri). We find that the two species are genetically distinct, based on levels of heterozygosity and patterns of allele sharing. Focusing on the western lowland population, we observe evidence for population substructure, and a deficit of rare genetic variants suggesting a recent episode of population contraction. In western lowland gorillas, there is an elevation of variation towards telomeres and centromeres on the chromosomal scale. On a finer scale, we find substantial variation in genetic diversity, including a marked reduction close to the major histocompatibility locus, perhaps indicative of recent strong selection there. These findings suggest that despite their maintaining an overall level of genetic diversity equal to or greater than that of humans, population decline, perhaps associated with disease, has been a significant factor in recent and long-term pressures on wild gorilla populations.

Observational Monitoring of Clinical Signs during the Last Stage of Habituation in a Wild Western Gorilla Group at Bai Hokou, Central African Republic

Anthropozoonotic disease transmission to great apes is a critical conservation concern, and has raised ethical doubts regarding ape habituation. We monitored over a 3-year period clinical signs within a group of wild western gorillas (G. gorilla) undergoing habituation at Bai Hokou, Central African Republic. The majority of observations consisted of singular coughs and sneezes among the gorillas. These were the only clinical signs that significantly and positively increased over the years. No changes in the demography of the study group were observed. While clinical signs are not necessarily indicative of ‘disease' or other health-related problems, we discuss how long-term records of clinical signs provide useful information when health monitoring, and the importance of the rigid application of preventive disease transmission protocols.

Leaf Surface Roughness Elicits Leaf Swallowing Behavior in Captive Chimpanzees (Pan troglodytes) and Bonobos (P. paniscus), but not in Gorillas (Gorilla gorilla) or Orangutans (Pongo abelii)

Researchers have described apparently self-medicative behaviors for a variety of nonhuman species including birds and primates. Wild chimpanzees, bonobos, and gorillas have been observed to swallow rough leaves without chewing, a behavior proposed to be self-medicative and to aid control of intestinal parasites. Researchers have hypothesized that the presence of hairs on the leaf surface elicits the behavior. We investigated the acquisition and the underlying mechanisms of leaf swallowing. We provided 42 captive great apes (24 chimpanzees, six bonobos, six gorillas, and six orangutans) with both rough-surfaced and hairless plants. None of the subjects had previously been observed to engage in leaf swallowing behavior and were therefore assumed naive. Two chimpanzees and one bonobo swallowed rough-surfaced leaves spontaneously without chewing them. In a social setup six more chimpanzees acquired the behavior. None of the gorillas or orangutans showed leaf swallowing. Because this behavior occurred in naive individuals, we conclude that it is part of the behavioral repertoire of chimpanzees and bonobos. Social learning is thus not strictly required for the acquisition of leaf swallowing, but it may still facilitate its expression. The fact that apes always chewed leaves of hairless control plants before swallowing, i.e., normal feeding behavior, indicates that the surface structure of leaves is indeed a determinant for initiating leaf swallowing in apes where it occurs.

Detecting intraannual dietary variability in wild mountain gorillas by stable isotope analysis of feces

We use stable isotope ratios in feces of wild mountain gorillas (Gorilla beringei) to test the hypothesis that diet shifts within a single year, as measured by dry mass intake, can be recovered. Isotopic separation of staple foods indicates that intraannual changes in the isotopic composition of feces reflect shifts in diet. Fruits are isotopically distinct compared with other staple foods, and peaks in fecal δ(13)C values are interpreted as periods of increased fruit feeding. Bayesian mixing model results demonstrate that, although the timing of these diet shifts match observational data, the modeled increase in proportional fruit feeding does not capture the full shift. Variation in the isotopic and nutritional composition of gorilla foods is largely independent, highlighting the difficulty for estimating nutritional intake with stable isotopes. Our results demonstrate the potential value of fecal sampling for quantifying short-term, intraindividual dietary variability in primates and other animals with high temporal resolution even when the diet is composed of C(3) plants.

Seasonal effects on great ape health: a case study of wild chimpanzees and Western gorillas.

Among factors affecting animal health, environmental influences may directly or indirectly impact host nutritional condition, fecundity, and their degree of parasitism. Our closest relatives, the great apes, are all endangered and particularly sensitive to infectious diseases. Both chimpanzees and western gorillas experience large seasonal variations in fruit availability but only western gorillas accordingly show large changes in their degree of frugivory. The aim of this study is to investigate and compare factors affecting health (through records of clinical signs, urine, and faecal samples) of habituated wild ape populations: a community (N = 46 individuals) of chimpanzees (Pan troglodytes) in Kanyawara, Kibale National Park (Uganda), and a western gorilla (G. gorilla) group (N = 13) in Bai Hokou in the Dzanga-Ndoki National Park (Central African Republic). Ape health monitoring was carried out in the wet and dry seasons (chimpanzees: July–December 2006; gorillas: April–July 2008 and December 2008–February 2009). Compared to chimpanzees, western gorillas were shown to have marginally greater parasite diversity, higher prevalence and intensity of both parasite and urine infections, and lower occurrence of diarrhea and wounds. Parasite infections (prevalence and load), but not abnormal urine parameters, were significantly higher during the dry season of the study period for western gorillas, who thus appeared more affected by the large temporal changes in the environment in comparison to chimpanzees. Infant gorillas were the most susceptible among all the age/sex classes (of both apes) having much more intense infections and urine blood concentrations, again during the dry season. Long term studies are needed to confirm the influence of seasonal factors on health and parasitism of these great apes. However, this study suggest climate change and forest fragmentation leading to potentially larger seasonal fluctuations of the environment may affect patterns of ape parasitism and further exacerbate health impacts on great ape populations that live in highly seasonal habitats.

Early Brain Growth Cessation in Wild Virunga Mountain Gorillas (Gorilla beringei beringei)

Understanding the life history correlates of ontogenetic differences in hominoid brain growth requires information from multiple species. At present, however, data on how brain size changes over the course of development are only available from chimpanzees and modern humans. In this study, we examined brain growth in wild Virunga mountain gorillas using data derived from necropsy reports (N = 34) and endocranial volume (EV) measurements (N = 86). The youngest individual in our sample was a 10-day-old neonatal male with a brain mass of 208 g, representing 42% of the adult male average. Our results demonstrate that Virunga mountain gorillas reach maximum adult-like brain mass by 3-4 years of age; adult-sized EV is reached by the time the first permanent molars emerge. This is in contrast to the pattern observed in chimpanzees, which despite their smaller absolute brain size, reportedly attain adult brain mass approximately 1 year later than Virunga mountain gorillas. Our findings demonstrate that brain growth is completed early in Virunga mountain gorillas compared to other great apes studied thus far, in a manner that appears to be linked with other life history characteristics of this population.

Treponemal Infection in Nonhuman Primates as Possible Reservoir for Human Yaws

Treponemal Infection in Nonhuman Primates as Possible Reservoir for Human Yaws

Non-invasive monitoring of physiological stress in the Western lowland gorilla (Gorilla gorilla gorilla): Validation of a fecal glucocorticoid assay and methods for practical application in the field

Enzymeimmunoassays (EIAs) allow researchers to monitor stress hormone output via measurement of fecal glucocorticoid metabolites (FGCMs) in many vertebrates. They can be powerful tools which allow the acquisition of otherwise unobtainable physiological information from both captive animals and wild animals in remote forest habitats, such as great apes. However, methods for hormone measurement, extraction and preservation need to be adapted and validated for field settings. In preparation for a field study of Western lowland gorillas (Gorilla gorilla gorilla) in the Central African Republic we used samples from captive gorillas collected around opportunistic stressful situations to test whether four different glucocorticoid EIAs reflected adrenocortical activity reliably and to establish the lag-time from the stressor to peak excretion. We also validated a field extraction technique and established a simple, non-freezer-reliant method to preserve FGCMs in extracts long-term. We determined the rate of FGCM change over 28days when samples cannot be extracted immediately and over 12h when feces cannot be preserved immediately in alcohol. Finally, we used repeat samples from identified individuals to test for diurnal variation in FGCM output. Two group-specific assays measuring major cortisol metabolites detected the predicted FGCM response to the stressor reliably, whereas more specific cortisol and corticosterone assays were distinctly less responsive and thus less useful. We detected a lag time of 2–3days from stressor to peak FGCM excretion. Our field extraction method performed as well as an established laboratory extraction method and FGCMs in dried extracts stored at ambient temperatures were as stable as those at −20°C over 1yr. Hormones in non-extracted feces in alcohol were stable up to 28days at ambient temperatures. FGCMs in un-fixed gorilla feces deteriorated to almost 50% of the original values within 6h under field conditions. We detected no diurnal variation in FGCMs in samples from wild gorillas. Our study highlights the importance of thorough biological and immunological validation of FGCM assays, and presents validated, practical methods for the application of non-invasive adrenocortical monitoring techniques to field conservation contexts where it is crucially needed.

Generation times in wild chimpanzees and gorillas suggest earlier divergence times in great ape and human evolution

Fossils and molecular data are two independent sources of information that should in principle provide consistent inferences of when evolutionary lineages diverged. Here we use an alternative approach to genetic inference of species split times in recent human and ape evolution that is independent of the fossil record. We first use genetic parentage information on a large number of wild chimpanzees and mountain gorillas to directly infer their average generation times. We then compare these generation time estimates with those of humans and apply recent estimates of the human mutation rate per generation to derive estimates of split times of great apes and humans that are independent of fossil calibration. We date the human-chimpanzee split to at least 7-8 million years and the population split between Neanderthals and modern humans to 400,000-800,000 y ago. This suggests that molecular divergence dates may not be in conflict with the attribution of 6- to 7-million-y-old fossils to the human lineage and 400,000-y-old fossils to the Neanderthal lineage.

Extending across continents: Travel medicine and Latin America

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 21 days 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 7 m 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.

In Vitro Fermentation of Dietary Carbohydrates Consumed by African Apes and Monkeys: Preliminary Results for Interpreting Microbial and Digestive Strategy

Primates derive significant nutritional benefits from hosting symbiotic, fermenting microbes in their gut, including the provision of energy from short-chain fatty acids (SCFAs). We measured fermentation parameters in fecal samples of 4 hindgut fermenting species (Gorilla gorilla, Pan troglodytes, Papio hamadryas, Cercopithecus neglectus) and 1 foregut fermenting species (Colobus guereza) to determine whether differences in SCFA profiles exist between the 2 digestive systems. We analyzed SCFA profiles, culture pH, and methane from fecal samples collected at the North Carolina Zoological Park. Results indicate that the captive individuals exhibit high total SCFA concentrations, with a particularly high acetate-to-propionate ratio. Methane levels were highest in the 2 ape species, and lowest in Colobus guereza and Cercopithecus neglectus. Total SCFA concentrations were similar between wild and captive-born Gorilla gorilla, although concentrations of acetate were significantly greater —and butyrate concentration and methane production significantly lower— in wild-caught gorillas relative to captive-born. These results are consistent with data on diet and digestive retention times among Catarrhini and have implications for our understanding of the interactions among diet, body mass, digestion, and how monogastric cercopithecines can consume either similar or greater levels of fiber than larger-bodied apes.

Consequences of Non-Intervention for Infectious Disease in African Great Apes

Infectious disease has recently joined poaching and habitat loss as a major threat to African apes. Both “naturally” occurring pathogens, such as Ebola and Simian Immunodeficiency Virus (SIV), and respiratory pathogens transmitted from humans, have been confirmed as important sources of mortality in wild gorillas and chimpanzees. While awareness of the threat has increased, interventions such as vaccination and treatment remain controversial. Here we explore both the risk of disease to African apes, and the status of potential responses. Through synthesis of published data, we summarize prior disease impact on African apes. We then use a simple demographic model to illustrate the resilience of a well-known gorilla population to disease, modeled on prior documented outbreaks. We found that the predicted recovery time for this specific gorilla population from a single outbreak ranged from 5 years for a low mortality (4%) respiratory outbreak, to 131 years for an Ebola outbreak that killed 96% of the population. This shows that mortality rates comparable to those recently reported for disease outbreaks in wild populations are not sustainable. This is particularly troubling given the rising pathogen risk created by increasing habituation of wild apes for tourism, and the growth of human populations surrounding protected areas. We assess potential future disease spillover risk in terms of vaccination rates amongst humans that may come into contact with wild apes, and the availability of vaccines against potentially threatening diseases. We discuss and evaluate non-interventionist responses such as limiting tourist access to apes, community health programs, and safety, logistic, and cost issues that constrain the potential of vaccination.

Assessing Initial Reintroduction Success in Long-Lived Primates by Quantifying Survival, Reproduction, and Dispersal Parameters: Western Lowland Gorillas (Gorilla gorilla gorilla) in Congo and Gabon

Postrelease monitoring is an important aspect of reintroduction projects, one outcome of which is to allow an assessment of the initial success of the reintroduction, often measured by quantifying survival and reproduction rates. In long-lived species, accurate estimations of demographic parameters are difficult to obtain, and therefore assessment of reintroduction success in such species is challenging. To assess the initial success of a reintroduction program for the long-lived, slow-reproducing, and critically endangered western lowland gorilla Gorilla gorilla gorilla, we analyzed postrelease monitoring data from 2 reintroduced populations, in the Bateke Plateau region of the Republics of Congo and Gabon, to quantify several demographic parameters, and compared our results with published data on wild gorilla populations. Annual survival rate of the 51 released gorillas was 97.4%, 9 females gave birth to 11 infants at an annual birth rate of 0.196 births per adult female, and first-year survival of the infants was 81.8%. Annual birth rate within the reintroduced populations is not significantly different from that given for wild western gorilla populations, and other demographic parameters fall within the range of published data for wild gorilla populations. Our analysis illustrates that the reintroduction program has been successful in terms of the initial measures of postrelease survival and reproduction, and our quantitative data should facilitate the development of a population model that can predict the probability of population persistence and therefore provide an indication of longer-term reintroduction success.