Free-ranging Mountain Gorillas Research Articles

Simian homologues of human herpesviruses and implications for novel viral introduction to free-living mountain gorillas.

The endangered mountain gorilla (Gorilla beringei beringei) in Rwanda, Uganda, and the Democratic Republic of Congo is frequently in contact with humans through tourism, research activities, and illegal entry of people into protected gorilla habitat. Herpesviruses, which are ubiquitous in primates, have the potential to be shared in any setting where humans and gorillas share habitat. Based on serological findings and clinical observations of orofacial ulcerated lesions resembling herpetic lesions, an alpha-herpesvirus resembling human herpes simplex virus type 1 (HSV-1) has long been suspected to be present in human-habituated mountain gorillas in the wild. While the etiology of orofacial lesions in the wild has not been confirmed, HSV-1 has been suspected in captively-housed mountain gorillas and confirmed in a co-housed confiscated Grauer's gorilla (Gorilla beringei graueri). To better characterize herpesviruses infecting mountain gorillas and to determine the presence/absence of HSV-1 in the free-living population, we conducted a population-wide survey to test for the presence of orally shed herpesviruses. DNA was extracted from discarded chewed plants collected from 294 individuals from 26 groups, and samples were screened by polymerase chain reaction using pan-herpesvirus and HSV-1-specific assays. We found no evidence that human herpesviruses had infected free-ranging mountain gorillas. However, we found gorilla-specific homologs to human herpesviruses, including cytomegaloviruses (GbbCMV-1 and 2), a lymphocryptovirus (GbbLCV-1), and a new rhadinovirus (GbbRHV-1) with similar characteristics (i.e., timing of primary infection, shedding in multiple age groups, and potential modes of transmission) to their human counterparts, human cytomegalovirus, Epstein-Barr virus and Kaposi's sarcoma-associated herpesvirus, respectively.

Pathological lesions of the digestive tract in free-ranging mountain gorillas (Gorilla beringei beringei).

The finding of parasites and bacterial pathogens in mountain gorilla feces and oral lesions in gorilla skeletal remains has not been linked to pathological evidence of morbidity or mortality. In the current study, we conducted a retrospective study of digestive tracts including oral cavity, salivary glands, esophagus, stomach, intestines (gastrointestinal tract [GI]), liver, and pancreas of 60 free-ranging mountain gorillas from Uganda, Rwanda, and the Democratic Republic of Congo that died between 1985 and 2007. We reviewed clinical histories and gross pathology reports and examined histological sections. On histology, enteritis (58.6%), gastritis (37.3%), and colitis (29.3%) were the commonest lesions in the tracts. Enteritis and colitis were generally mild, and judged likely to have been subclinical. Gastritis was often chronic and proliferative or ulcerative, and associated with nematodiasis. A gastro-duodenal malignancy (carcinoid) was present in one animal. A number of incidental lesions were identified throughout the tract and cestodes and nematodes were frequently observed grossly and/or histologically. Pigmentation of teeth and tongue were a common finding, but periodontitis and dental attrition were less common than reported from past studies of skeletal remains. Despite observing numerous GI lesions and parasites in this study of deceased free-living mountain gorillas, we confirmed mortality attributable to gastroenteritis in just 8% (5/60) cases, which is less than that described in captive gorillas. Other deaths attributed to digestive tract lesions included cleft palate in an infant, periodontal disease causing systemic infection in an older adult and gastric cancer. Of all the parasitic infections observed, only hepatic capillariasis and gastric nematodiasis were significantly associated with lesions (hepatitis and gastritis, respectively). Understanding GI lesions in this endangered species is key in the management of morbidity associated with GI ailments.

Human Respiratory Syncytial Virus Detected in Mountain Gorilla Respiratory Outbreaks

Respiratory illness (RI) accounts for a large proportion of mortalities in mountain gorillas (Gorilla beringei beringei), and fatal outbreaks, including disease caused by human metapneumovirus (HMPV) infections, have heightened concern about the risk of human pathogen transmission to this endangered species, which is not only critically important to the biodiversity of its ecosystem but also to the economies of the surrounding human communities. Our goal was to conduct a molecular epidemiologic study to detect the presence of HRSV and HMPV in fecal samples from wild human-habituated free-ranging mountain gorillas in Rwanda and to evaluate the role of these viruses in RI outbreaks. Fecal samples were collected from gorillas with clinical signs of RI between June 2012 and February 2013 and tested by real-time and conventional polymerase chain reaction (PCR) assays; comparison fecal samples were obtained from gorillas without clinical signs of RI sampled during the 2010 Virunga gorilla population census. PCR assays detected HMPV and HRSV first in spiked samples; subsequently, HRSV-A, the worldwide-circulating ON1 genotype, was detected in 12 of 20 mountain gorilla fecal samples collected from gorillas with RI during outbreaks, but not in samples from animals without respiratory illness. Our findings confirmed that pathogenic human respiratory viruses are transmitted to gorillas and that they are repeatedly introduced into mountain gorilla populations from people, attesting to the need for stringent biosecurity measures for the protection of gorilla health.

Noninvasive Saliva Collection Techniques for Free-Ranging Mountain Gorillas and Captive Eastern Gorillas

This study was designed to develop a simple, noninvasive method for saliva collection: a first step toward developing new diagnostic tests to survey gorillas for infectious diseases. The subjects included free-ranging mountain gorillas (Gorilla beringei beringei) in the Parc National des Volcans, Rwanda, and a group of orphan mountain and Grauer's gorillas (Gorilla heringei graueri) housed nearby in a temporary holding facility. Three collection methods were used to recover saliva from discarded forest food: swabbing, soaking, and washing. Saliva was also collected from orphan gorillas maintained in a captive setting by using dental ropes inside mesh bags. The presence of gorilla saliva in each sample was confirmed by using a salivary s-amylase assay and forensic press test paper. The recovery of gorilla DNA was verified by polymerase chain reaction by using primers specific to mountain and Grauer's gorillas. Of the three collection techniques used to recover saliva from forest food, directly swabbing plant bite marks was the most effective. Wild celery (Peucedanum linderi) provided for the most consistent saliva recovery and is eaten year round by mountain gorillas in Rwanda. This study shows that gorilla saliva can be recovered easily and noninvasively from known individual free-ranging gorillas by collecting pieces of wild celery discarded as the gorillas forage and from captive gorillas by offering them juice-soaked dental ropes inside mesh bags. Both methods can be used to recover gorilla DNA for genetic studies. Saliva collected from free-ranging and captive gorillas may prove to be a useful biologic sample for the development of new diagnostic tests and hormonal analysis.

CHOLESTEROL VALUES IN FREE-RANGING GORILLAS (GORILLA GORILLA GORILLA AND GORILLA BERINGEI) AND BORNEAN ORANGUTANS (PONGO PYGMAEUS)

Cholesterol concentrations in captive gorillas and orangutans vary widely within species and average approximately 244 mg/dl for gorillas and 169 mg/dl for orangutans as published previously. The International Species Inventory System reports higher concentrations of 275 and 199 mg/dl for gorillas and orangutans, respectively. It is unknown whether these values were typical, influenced by captive management, or both. To answer this question, banked serum samples from free-ranging mountain gorillas (Gorilla beringei), western lowland gorillas (Gorilla gorilla gorilla), and Bornean orangutans (Pongo pygmaeus) were analyzed for total cholesterol, triglyceride, high-density lipoprotein cholesterol, and low-density lipoprotein cholesterol concentrations. Mountain gorillas did not differ significantly from free-ranging western lowland gorillas in cholesterol, triglyceride, high-density lipoprotein cholesterol, or low-density lipoprotein cholesterol concentrations, indicating mountain gorilla values could be a model for western lowland gorillas. Captive gorilla total cholesterol and low-density lipoprotein cholesterol concentrations were significantly higher (P < 0.05) than in free-ranging groups. Triglyceride concentrations for captive gorillas were significantly higher (P < 0.05) than the male mountain and western lowland gorillas, but they were not significantly different from the female mountain gorillas. Captive orangutan total cholesterol concentrations were only higher (P < 0.05) than the free-ranging female orangutans, whereas captive orangutan low-density lipoprotein cholesterol concentrations were significantly higher (P < 0.05) than both free-ranging male and female orangutans. Calculated and measured low-density lipoprotein cholesterol concentrations were compared for all free-ranging animals and were significantly different (P < 0.05) for all groups, indicating Friedewald's equation for calculating low-density lipoprotein cholesterol is not appropriate for use with nonfasted apes. The higher total cholesterol and low-density lipoprotein cholesterol concentrations in captive apes may predispose them to cardiovascular disease and might be attributed to diets, limited energy expenditure, and genetics.

Anthropozoonotic Giardia duodenalis genotype (assemblage) a infections in habitats of free-ranging human-habituated gorillas, Uganda.

To facilitate ecotourism and research, free-ranging mountain gorillas of Uganda have been habituated to humans. Testing of fecal samples of gorillas (n = 100), people sharing gorilla habitats (n = 62). and local pre- and postweaned cattle (n = 50) having access to these habitats with fluorescein isothiocyanate-conjugated monoclonal antibodies revealed Giardia duodenalis cysts at prevalences of 2, 5, and 10%, respectively. The identification of G. duodenalis was confirmed by fluorescent in situ hybridization with 2 species-specific 18-bp oligonucleotide probes conjugated to hexachlorinated 6-carboxyfluorescein. The mean pathogen concentration was 2.5, 2.8, and 0.2 x 10(4) cysts/g of the gorilla, people, and cattle feces, respectively. All cyst isolates aligned with genotype (assemblage) A, as confirmed by polymerase chain reaction amplification and sequencing of a 130-bp region near the 5' end of the small subunit-ribosomal RNA gene. A single genotype (assemblage) A recovered from 3 genetically distant but geographically united host groups indicates anthropozoonotic transmission of G. duodenalis. A large percentage of the local community does not follow park regulations regarding the disposal of their fecal waste, as self-reported in a questionnaire. This genotype may have been introduced into gorilla populations through habituation activities and may have then been sustained in their habitats by anthropozoonotic transmission.

Cryptosporidiosis in people sharing habitats with free-ranging mountain gorillas (Gorilla gorilla beringei), Uganda.

Cryptosporidiosis, a zoonotic diarrheal disease, significantly contributes to the mortality of people with impaired immune systems worldwide. Infections with an animal-adapted genotype (Genotype 2) of Cryptosporidium parvum were found in a human population in Uganda that shares habitats with free-ranging gorillas, from which the same genotype of C. parvum had been recovered previously. A high prevalence of disease was found in park staff members (21%) who frequently contact gorillas versus 3% disease prevalence in the local community. This indicates a zoonotic transmission cycle of this pathogen against which no effective prophylaxis or therapy exists. The results of the study questionnaire demonstrated a high percentage of people not undertaking appropriate precautions to prevent fecal-oral transmission of C. parvum in the Bwindi Impenetrable National Park, Uganda. This human population will benefit from stronger compliance with park regulations regarding disposal of their fecal waste within the park boundaries.

Scabies in free-ranging mountain gorillas (Gorilla beringei beringei) in Bwindi Impenetrable National Park, Uganda

Between August and December 1996, there was an outbreak of a debilitating skin disease attributed to Sarcoptes scabiei infection in mountain gorillas (Gorilla beringei beringei) in Bwindi Impenetrable National Park...

Hyperkeratotic mange caused by Sarcoptes scabiei (Acariformes: Sarcoptidae) in juvenile human-habituated mountain gorillas (Gorilla gorilla beringei).

To facilitate ecotourism and behavioral research, free-ranging mountain gorillas (Gorilla gorilla beringei) have been habituated to humans. During routine health monitoring, five juvenile gorillas were observed with active crusted dermatitis and alopecia. Papular and vesicular lesions and crusts with papular eruption and oozing were numerous and disseminated over the body of one gorilla with a confirmed infestation of scabies. In this gorilla, the hyperkeratotic crusts were loose and thick with a flaky and scaly appearance. Histologically, the epidermis was thickened, displayed hyperkeratosis and was infiltrated with lymphocytes and neutrophils. Examination of skin scraping yielded a positive identification of adults and eggs of Sarcoptes scabiei mites. The gorillas were treated with ivermectin, 200 mg kg(-1). As S. scabiei mites can cross-infect various mammalian species causing self-limiting dermatitis, these ectoparasites can be propagated in the habitats shared by gorillas, people, and livestock, and therefore they represent an anthropozoonotic threat.

Campylobacteriosis, salmonellosis, and shigellosis in free-ranging human-habituated mountain gorillas of Uganda.

For conservation purposes and due to growing ecotourism, free-ranging mountain gorillas (Gorilla gorilla beringei) have been habituated to humans. Fecal specimens (n = 62) collected in January 1999 from mountain gorillas of the Bwindi and Mgahinga National Parks, Uganda, were tested for Campylobacter spp., Salmonella spp., and Shigella spp., and the overall prevalence of infection was 19%, 13%, and 6%, respectively. The prevalence of positive specimens was not related to the year of habituation of a gorilla group to humans. Campylobacter spp., Salmonella, and Shigella spp. infections were not distributed equally among the age classes of gorillas; most of the enteropathogens (80%), and all Shigella spp. organisms, S. sonnei, S. boydii, and S. flexneri, were isolated from subadults and adult gorillas with ages ranging from 6.0 to 11.9 yr. The prevalence of Campylobacter spp. and Salmonella spp. infections among human-habituated gorillas has doubled during the last 4 yr, and isolation of Shigella spp. for the first time from mountain gorillas, may indicate enhanced anthropozoonotic transmission of these enteropathogens.

Cryptosporidium parvum genotype 2 infections in free-ranging mountain gorillas (Gorilla gorilla beringei) of the Bwindi Impenetrable National Park, Uganda.

For behavioral research and due to growing ecotourism, some populations of free-ranging mountain gorillas (Gorilla gorilla beringei) have become habituated to humans. Molecular analysis of two Cryptosporidium sp. oocyst isolates originating from two human-habituated gorilla groups and two oocyst isolates from non-habituated gorillas yielded positive identification of C. parvum Genotype 2 (G2; i.e., "cattle", "animal-adapted", or "zoonotic"). As G2 is cross-transmissible between humans and animals, C. parvum infections can be propagated in the habitats of human-habituated, free-ranging gorillas through both zoonotic and anthroponotic transmission cycles.

A Demographic Analysis of Male Life History and Social Structure of Mountain Gorillas

AbstractTwenty-five years of demographic data on free-ranging mountain gorillas (Gorilla gorilla beringei) from the Karisoke Research Center, Rwanda were used to assess male life histories and the variation within the age-graded social structure. Group types include lone silver-backs, one-male, multimale, and all-male groups. Although 60% of gorilla groups in the Virunga population are one-male, a multimale structure may increase chances of survival and future reproductive success for males at three stages of their lives. Infants born in one-male groups appear more likely to die from infanticide than those in multimale groups. Immature males in one-male groups may face decreased future reproductive opportunities compared to males in multimale groups. Adult males in one-male groups lack possible partners for coalition formation during intergroup encounters. Demographic constraints, such as length of time to male maturation, coupled with intense male-male competition for mates may limit the number and duration of groups with a multimale structure. Individuals are not restricted to one group type for their entire adult lives and males that attain maturity in each group type may eventually reproduce. Variation in male reproductive success is based both on length of reproductive tenure and on the number of mates.

Diurnal urinary corticoid excretion in the human and gorilla.

Urinary corticoids were measured in humans (n = 9) in frequently collected urine samples taken during a 48 hr period, and in captive western lowland gorillas (n = 5) and free-ranging mountain gorillas (n = 3) from samples taken from 0700 to 1800 hr. In each study, the highest concentrations occurred in the morning hours, then declined gradually, reaching the lowest levels in the afternoon to evening. These data show that a similar diurnal pattern of corticoid excretion does occur in these species. We suggest that if single-sample urine collection for determination of hyperadrenal activity is to be used, urine is best collected during hours of low corticoid excretion. © 1994 Wiley-Liss, Inc.

Movement patterns of a group of free-ranging mountain gorillas (Gorilla gorilla beringei) and their relation to food availability.

Relationships between the movement patterns of free-ranging mountain gorillas (Gorilla gorilla beringei) and the abundance and distribution of foods in their home range were examined. During an 18-month field study, the ranging of one group of G. gorilla beringei was recorded on a 250 × 250 m grid system, from which measurements of frequency and duration of use, travel rate, and rate of revisitation of each quadrangle by the group were derived. Food items were sampled in selected quadrangles throughout the home range and various measures of food abundance, frequency and diversity were calculated. Analyses based on both spatial and temporal variation in food availability give supporting evidence for the prediction that mountain gorilla ranging patterns are influenced by the distribution and abundance of foods. Quality of food appears to be an important factor, as shown in analyses of yearly patterns and monthly changes in ranging. The gorillas studied spent more time in the higher quality areas of their home range, responded to a correlate of decreasing food abundance by increasing their rate of travel and area used, and revisited regions more frequently when the renewal rate of foods was clearly greater. Each of their foraging tactics can be explained as serving to increase the efficiency of harvesting foods.