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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.

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.

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.

Conservation efforts have led to the recovery of the endangered mountain gorilla populations. Due to their limited potential for spatial expansion, population densities increased, which may alter the epidemiology of infectious diseases. Recently, clinical gastrointestinal illnesses linked to helminth infections have been recorded in both gorilla populations. To understand drivers and patterns of helminth infections we quantified strongylid and tapeworm infections across both Virunga Massif and Bwindi populations using fecal egg counts. We assessed the impact of age, sex, group size, season and spatial differences used as a proxy, which reflects observed variation in the occurrence of gastrointestinal problems, vegetation types, gorilla subpopulation growth and associated social structure on helminth infections. We revealed striking geographic differences in strongylid infections with higher egg counts mostly in areas with high occurrences of gastrointestinal disease. Increased helminth egg counts were also associated with decreasing group size in some areas. Observed spatial differences may reflect mutual effects of variations in subpopulation growth rates, gorilla social structure, and vegetation associated with altitude across mountain gorilla habitat. Helminth infection intensities in Virunga gorillas were lowest in the youngest and the oldest animals. Elucidating parasite infection patterns of endangered species with low genetic diversity is crucial for their conservation management.

The future of primates depends on conservationists in primate range countries having the education and opportunities needed to facilitate conservation efforts. However, most primates are found in countries where conservation is underfunded. Rwanda is home to 14 primate species, with three being listed as endangered on the International Union for Conservation of Nature (IUCN) Red List. Their remaining native habitats are scarce, highly fragmented, and surrounded by high human densities. Lacking education opportunities and the loss of qualified individuals following decades of political instability created a need for well-trained conservationists to tackle conservation challenges in Rwanda. The Memoirs Program, a science capacity-building partnership between Dian Fossey Gorilla Fund (DFGF), University of Rwanda (UR), the Rwanda Development Board, and Cleveland Metroparks Zoo, aims to train the next generation of Rwandan conservationists. Annually, the Memoirs Program provides 10-12 top students from the UR Conservation Biology undergraduate program the opportunity to conduct senior research projects (Memoirs) at DFGF addressing conservation issues in and around Rwanda's protected areas. Students receive one-on-one supervision by DFGF scientists and affiliates to supplement UR mentorship, along with targeted teaching modules that reinforce and complement UR curricula. In continuation of the Memoirs Program, participants are offered professional development, employment opportunities, and support to publish their research in peer-reviewed journals. Since inception of the Program in 2003, 123 students have participated with 83% being employed or pursuing higher education degrees in conservation-related fields in Rwanda and the region. Pre- and post-training comparison of oral presentation skills, one of the teaching modules, involving 22 students demonstrated increased post-training performance. The Memoirs Program represents an effective partnership between the government, an international conservation non-governmental organization, and a public higher-learning institution in a developing country to support high-performing students to become tomorrow's conservation leaders. This model could be replicated within Rwanda and in other regions of the world.

Increasing population density can increase infectious disease risk and thus reduce population growth and size. Host-parasite interactions of threatened animals that remain in small protected forest fragments therefore need to be monitored carefully. Due to extreme conservation efforts, the mountain gorilla (Gorilla beringei beringei) population in the 450-km

Fleas (Siphonaptera) are ubiquitous blood-sucking parasites that transmit a range of vector-borne pathogens. The present study examined rodents (n = 29) and domestic dogs (n = 7) living in the vicinity of the Volcanoes National Park, Rwanda, for fleas, identified flea species from these hosts, and detected Bartonella (Rhizobiales: Bartonellaceae) and Rickettsia (Rickettsiales: Rickettsiaceae) DNA. The most frequently encountered flea on rodents was Xenopsylla brasiliensis (Siphonaptera: Pulicidae). In addition, Ctenophthalmus (Ethioctenophthalmus) calceatus cabirus (Siphonaptera: Hystrichopsyllidae) and Ctenocephalides felis strongylus (Siphonaptera: Pulicidae) were determined using morphology and sequencing of the cytochrome c oxidase subunit I and cytochrome c oxidase subunit II genes (cox1 and cox2, respectively). Bartonella tribocorum DNA was detected in X. brasiliensis and Rickettsia asembonensis DNA (a Rickettsia felis-like organism) was detected in C. felis strongylus. The present work complements studies that clarify the distributions of flea-borne pathogens and potential role of fleas in disease transmission in sub-Saharan Africa. In the context of high-density housing in central sub-Saharan Africa, the detection of B. tribocorum and R. asembonensis highlights the need for surveillance in both rural and urban areas to identify likely reservoirs.

Objectives Ecological factors, but also tooth-to-tooth contact over time, have a dramatic effect on tooth wear in primates. The aim of this study is to test whether incisor tooth wear changes predictably with age and can thus be used as an age estimation method in a wild population of mountain gorillas (Gorilla beringei beringei) from Volcanoes National Park, Rwanda. Materials and methods In mountain gorillas of confidently known chronological age (N = 24), we measured the crown height of all permanent maxillary and mandibular incisors (I1 , I1 , I2 , I2 ) as a proxy for incisal macrowear. Linear and quadratic regressions for each incisor were used to test whether age can be predicted by crown height. Using these models, we then predicted age at death of two individual mountain gorillas of probable identifications, based on their incisor crown height. Results Age decreased significantly with incisor height for all teeth, but the upper first incisors (I1 ) provided the best results, with the lowest Akaike's Information Criterion corrected for small sample size (AICc) and lowest Standard Error of the Estimate (SEE). When the best age equations for each sex were applied to gorillas with probable identifications, the predicted ages differed 1.58 and 3.33 years from the probable ages of these individuals. Conclusions Our findings corroborate that incisor crown height, a proxy for incisal wear, varies predictably with age. This relationship can be used to estimate age at death of unknown gorillas in the skeletal collection, and in some cases, to corroborate the identity of individual gorillas recovered from the forest postmortem at an advanced state of decomposition. Such identifications help fill gaps in the demographic database and support research that requires individual-level data.

Deeper or more ‘severe’ linear enamel hypoplasia (LEH) defects are hypothesized to reflect more severe stress during development, but it is not yet clear how depth is influenced by intrinsic enamel growth patterns. Recent work documented inter- and intraspecific differences in LEH defect depth in extant great apes, with mountain gorillas having shallower defects than other taxa, and females having deeper defects than males. Here, we assess the correspondence of inter- and intraspecific defect depth and intrinsic aspects of enamel growth: enamel extension rates, outer enamel striae of Retzius angles, and linear enamel thickness. Thin sections of great ape canines (n = 40) from Gorilla beringei beringei, Gorilla gorilla gorilla, Pan troglodytes, and Pongo spp. were analyzed. Enamel extension rates were calculated within deciles of enamel-dentine junction length. Linear enamel thickness and the angle of intersection between striae of Retzius and the outer enamel surface were measured in the imbricational enamel. Mountain gorillas have faster enamel extension rates and shallower striae angles than the other taxa examined. Mountain gorillas have thinner imbricational enamel than western lowland gorillas and orangutans, but not chimpanzees. In the combined-taxon sample, females exhibit larger striae angles and thicker imbricational enamel than males. Enamel extension rates are highly negatively correlated with striae angles and LEH defect depth. Enamel growth variation corresponds with documented inter- and intraspecific differences in LEH defect depth in great ape canines. Mountain gorillas have shallower striae angles and faster extension rates than other taxa, which might explain their shallow LEH defect morphology and the underestimation of their LEH prevalence in previous studies. These results suggest that stressors of similar magnitude and timing might produce defects of different depths in one species or sex vs. another, which has implications for interpretations of stress histories in hominins with variable enamel growth patterns.

OBJECTIVE Linear enamel hypoplasia (LEH) is a condition marked by localized reductions in enamel thickness, resulting from growth disruptions during dental development. We use quantitative criteria to characterize the depth of LEH defects and "normal" perikymata in great apes. We test the hypothesis that mountain gorillas have shallow defects compared to other taxa, which may have led to their underestimation in previous studies. MATERIALS AND METHODS Previous attempts to characterize LEH morphology quantitatively have been limited in sample size and scope. We generated digital elevation models using optical profilometry (Sensofar PLu Neox) and extracted 2D coordinates using ImageJ to quantify depths in canines from three great ape genera (N = 75 perikymata; 255 defects). RESULTS All defect depths fall outside the distribution of perikymata depths. Mountain gorilla defects are significantly shallower than those of other great ape taxa examined, including western lowland gorillas. Females have significantly deeper defects than males in all taxa. The deepest defect belongs to a wild-captured zoo gorilla. Virunga mountain gorilla specimens collected by Dian Fossey exhibit deeper defects than those collected recently. DISCUSSION Shallow defect morphology in mountain gorillas may have led to an underestimation of LEH prevalence in past studies. Defect depth is used as a proxy for insult severity, but depth might be influenced by inter- and intra-specific variation in enamel growth. Future studies should test whether severe insults are associated with deeper defects, as might be the case with Haloko, a wild-captured gorilla. Ongoing histologic studies incorporating associated behavioral records will test possible factors that underlie differences in defect morphology.

Objectives While dental development is important to life history investigations, data from wild known-aged great apes are scarce. We report on the first radiographic examination of dental development in wild Virunga mountain gorillas, using known-age skeletal samples recovered in Rwanda. Materials and methods In 43 individuals (0.0–14.94 years), we collected radiographs of mandibular molars, and where possible, cone beam CT scans. Molar crown and root calcification status was assessed using two established staging systems, and age prediction equations generated using polynomial regression. Results were compared to available data from known-age captive and wild chimpanzees. Results Mountain gorillas generally fell within reported captive chimpanzee distributions or exceeded them, exhibiting older ages at equivalent radiographic stages of development. Differences reflect delayed initiation and/or an extended duration of second molar crown development, and extended first and second molar root development, in mountain gorillas compared to captive chimpanzees. However, differences in the duration of molar root development were less evident compared to wild chimpanzees. Discussion Despite sample limitations, our findings extend the known range of variation in radiographic estimates of molar formation timing in great apes, and provide a new age prediction technique based on wild specimens. However, mountain gorillas do not appear accelerated in radiographic assessment of molar formation compared to chimpanzees, as they are for other life history traits. Future studies should aim to resolve the influence of species differences, wild versus captive environments, and/or sampling phenomena on patterns observed here, and more generally, how they relate to variation in tooth size, eruption timing, and developmental life history.

Bats living in close contact with people in Rwanda were tested for evidence of infection with viruses of zoonotic potential. Mucosal swabs from 503 bats representing 17 species were sampled from 2010 to 2014 and screened by consensus PCR for 11 viral families. Samples were negative for all viral families except coronaviruses, which were detected in 27 bats belonging to eight species. Known coronaviruses detected included the betacorona viruses: Kenya bat coronaviruses, Eidolon bat coronavirus, and Bat coronavirus HKU9, as well as an alphacoronavirus, Chaerephon Bat coronavirus. Novel coronaviruses included two betacorona viruses clustering with SARS-CoV, a 2d coronavirus, and an alphacoronavirus.

Eastern gorillas ( Gorilla beringei ) are among the few mammal species that seasonally consume large quantities of young bamboo shoots, which are a rich source of energy. Here, we document how the consumption of bamboo shoots coincides with changes in behavior of adult mountain gorillas ( Gorilla beringei beringei ) monitored by the Dian Fossey Gorilla Fund’s Karisoke Research Center in Volcanoes National Park, Rwanda. We offer a preliminary analysis of possible mechanisms underlying this behavioral change by measuring energy intake rates and the presence of cyanide and alcohol—ingredients potentially associated with increased activity levels—in fresh bamboo shoots. The percentage of bamboo shoots in the diet of gorillas was correlated positively with the rate of play behavior shown by adults in 2 of the 3 study groups. Play behavior was not the result of better weather conditions and also did not reflect the availability of spare time. Rather, there is some, but not consistent, evidence for a link between energy intake rates and play behavior of adults. Cyanide was not detected in young bamboo shoots, and the presence of alcohol remains inconclusive, albeit unlikely. In sum, our results show that consumption of a high-quality food can have a direct influence on the activity budget (and by extrapolation energy expenditure) of mountain gorillas through increased rates of play behavior. However, the physiological aspects underlying this elevated activity warrant further investigation.

Infectious diseases pose one of the most significant threats to the survival of great apes in the wild. The critically endangered mountain gorilla (Gorilla beringei beringei) is at high risk for contracting human pathogens because approximately 60% of the population is habituated to humans to support a thriving ecotourism program. Disease surveillance for human and non-human primate pathogens is important for population health and management of protected primate species. Here, we evaluate discarded plants from mountain gorillas and sympatric golden monkeys (Cercopithecus mitis kandti), as a novel biological sample to detect viruses that are shed orally. Discarded plant samples were tested for the presence of mammalian-specific genetic material and two ubiquitous DNA and RNA primate viruses, herpesviruses, and simian foamy virus. We collected discarded plant samples from 383 wild human-habituated mountain gorillas and from 18 habituated golden monkeys. Mammalian-specific genetic material was recovered from all plant species and portions of plant bitten or chewed by gorillas and golden monkeys. Gorilla herpesviral DNA was most consistently recovered from plants in which leafy portions were eaten by gorillas. Simian foamy virus nucleic acid was recovered from plants discarded by golden monkeys, indicating that it is also possible to detect RNA viruses from bitten or chewed plants. Our findings show that discarded plants are a useful non-invasive sampling method for detection of viruses that are shed orally in mountain gorillas, sympatric golden monkeys, and potentially other species. This method of collecting specimens from discarded plants is a new non-invasive sampling protocol that can be combined with collection of feces and urine to evaluate the most common routes of viral shedding in wild primates. Am. J. Primatol. 78:1222-1234, 2016. © 2016 Wiley Periodicals, Inc.

Objectives Great ape teeth must remain functional over long lifespans. The molars of the most folivorous apes, the mountain gorillas, must maintain shearing function for 40+ years while the animals consume large quantities of mechanically challenging foods. While other folivorous primates experience dental senescence, which compromises their occlusal surfaces and affects their reproductive success as they age, it is unknown whether dental senescence also occurs in mountain gorillas. In this article, we quantified and evaluated how mountain gorilla molars change throughout their long lifespans. Materials and methods We collected high-resolution replicas of M(1)s (n = 15), M(2)s (n = 13), and M(3)s (n = 11) from a cross-sectional sample of wild mountain gorilla skeletons from the Virunga Volcanoes, ranging in age from 4 to 43 years. We employed dental topographic analyses to track how aspects of occlusal slope, angularity, relief index, and orientation patch count rotated change with age. In addition, we measured the relative length of shearing crests in two- and three-dimensions. Results Occlusal topography was found to decrease, while 2D relative shearing crest length increased, and 3D relative crest lengths were maintained with age. Discussion Our findings indicate that shearing function is maintained throughout the long lifetimes of mountain gorillas. Unlike the dental senescence experienced by other folivorous primates, mountain gorillas do not appear to possess senesced molars despite their long lifetimes, mechanically challenging diets, and decreases in occlusal topography with age.

Bone loss and heightened fracture risk are common conditions associated with ageing in modern human populations and have been attributed to both hormonal and other metabolic and behavioural changes. To what extent these age-related trends are specific to modern humans or generally characteristic of natural populations of other taxa is not clear. In this study, we use computed tomography to examine age changes in long bone and vertebral structural properties of 34 wild-adult Virunga mountain gorillas ( Gorilla beringei beringei ) whose skeletons were recovered from natural accumulations. Chronological ages were known or estimated from sample-specific dental wear formulae and ranged between 11 and 43 years. Gorillas show some of the same characteristics of skeletal ageing as modern humans, including endosteal and some periosteal expansion. However, unlike in humans, there is no decline in cortical or trabecular bone density, or in combined geometric-density measures of strength, nor do females show accelerated bone loss later in life. We attribute these differences to the lack of an extended post-reproductive period in gorillas, which provides protection against bone resorption. Increases in age-related fractures (osteoporosis) in modern humans may be a combined effect of an extended lifespan and lower activity levels earlier in life. This article is part of the theme issue ‘Evolution of the primate ageing process'.

Mountain gorillas ( Gorilla beringei beringei) are one of the most critically endangered great apes in the world. The most common cause of mountain gorilla morbidity and mortality is trauma (e.g., injury from conspecifics or snare entrapment). We conducted a retrospective case-control study of free-ranging, human-habituated mountain gorillas to evaluate factors associated with snare entrapment and the results of clinical intervention. Data were collected from clinical records on all clinical intervention cases ( n=132) in Volcanoes National Park, Rwanda, conducted between 1995-2015. Wildlife veterinarians treated 37 gorillas entrapped in snares and 95 gorillas for other clinical conditions (including trauma and respiratory illness). Multivariate statistical analyses revealed that young gorillas (8 yr old) were more likely than older gorillas to become snared; that comorbidities delayed times to intervention (≥3 d); and that severity of wounds at the time of intervention were associated with increased risk of lasting impairment (including loss of limb or limb function, or death) within 1 mo after intervention. Our results may influence decisions for gorilla health monitoring and treatment to most effectively conserve this critically endangered species.

Epstein-Barr virus (EBV) infects greater than 90% of humans, is recognized as a significant comorbidity with HIV/AIDS, and is an etiologic agent for some human cancers. The critically endangered mountain gorilla population was suspected of infection with an EBV-like virus based on serology and infant histopathology similar to pulmonary reactive lymphoid hyperplasia (PRLH), a condition associated with EBV in HIV-infected children. To further examine the presence of EBV or an EBV-like virus in mountain gorillas, we conducted the first population-wide survey of oral samples for an EBV-like virus in a nonhuman great ape. We discovered that mountain gorillas are widely infected (n = 143/332) with a specific strain of lymphocryptovirus 1 (GbbLCV-1). Fifty-two percent of infant mountain gorillas were orally shedding GbbLCV-1, suggesting primary infection during this stage of life, similar to what is seen in humans in less developed countries. We then identified GbbLCV-1 in post-mortem infant lung tissues demonstrating histopathological lesions consistent with PRLH, suggesting primary infection with GbbLCV-1 is associated with PRLH in infants. Together, our findings demonstrate that mountain gorilla’s infection with GbbLCV-1 could provide valuable information for human disease in a natural great ape setting and have potential conservation implications in this critically endangered species.

Objectives The effects of phylogeny and locomotor behavior on long bone structural proportions are assessed through comparisons between adult and ontogenetic samples of extant gorillas. Materials and Methods A total of 281 wild-collected individuals were included in the study, divided into four groups that vary taxonomically and ecologically: western lowland gorillas (G. g. gorilla), lowland and highland grauer gorillas (G. b. graueri), and Virunga mountain gorillas (G. b. beringei). Lengths and articular breadths of the major long bones (except the fibula) were measured, and diaphyseal cross-sectional geometric properties determined using computed tomography. Ages of immature specimens (n = 145) were known or estimated from dental development. Differences between groups in hind limb to forelimb proportions were assessed in both adults and during development. Results Diaphyseal strength proportions among adults vary in parallel with behavioral/ecological differences, and not phylogeny. The more arboreal western lowland and lowland grauer gorillas have relatively stronger forelimbs than the more terrestrial Virunga mountain gorillas, while the behaviorally intermediate highland grauer gorillas have intermediate proportions. Diaphyseal strength proportions are similar in young infants but diverge after 2 years of age in western lowland and mountain gorillas, at the same time that changes in locomotor behavior occur. There are no differences between groups in length or articular proportions among either adults or immature individuals. Conclusion Long bone diaphyseal strength proportions in gorillas are developmentally plastic, reflecting behavior, while length and articular proportions are much more genetically canalized. These findings have implications for interpreting morphological variation among fossil taxa.

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.

We describe an atypical neuroanatomical feature present in several primate species that involves a fusion between the temporal lobe (often including Heschl's gyrus in great apes) and the posterior dorsal insula, such that a portion of insular cortex forms an isolated pocket medial to the Sylvian fissure. We assessed the frequency of this fusion in 56 primate species (including apes, Old World monkeys, New World monkeys, and strepsirrhines) by using either magnetic resonance images or histological sections. A fusion between temporal cortex and posterior insula was present in 22 species (seven apes, two Old World monkeys, four New World monkeys, and nine strepsirrhines). The temporoinsular fusion was observed in most eastern gorilla (Gorilla beringei beringei and G. b. graueri) specimens (62% and 100% of cases, respectively) but was seen less frequently in other great apes and was never found in humans. We further explored the histology of this fusion in eastern gorillas by examining the cyto- and myeloarchitecture within this region and observed that the degree to which deep cortical layers and white matter are incorporated into the fusion varies among individuals within a species. We suggest that fusion between temporal and insular cortex is an example of a relatively rare neuroanatomical feature that has become more common in eastern gorillas, possibly as the result of a population bottleneck effect. Characterizing the phylogenetic distribution of this morphology highlights a derived feature of these great apes.

Long-term studies of morbidity and mortality in free-ranging primates are scarce, but may have important implications for the conservation of extant populations. Infants comprise a particularly important age group, as variation in survival rates may have a strong influence on population dynamics. Since 1968, the Mountain Gorilla Veterinary Project (MGVP, Inc.) and government partners have conducted a comprehensive health monitoring and disease investigation program on mountain gorillas (Gorilla beringei beringei) in Rwanda, Uganda, and the Democratic Republic of the Congo. In an effort to better understand diseases in this species, we reviewed reliable field reports (n = 37), gross post-mortem (n = 66), and histopathology (n = 53) reports for 103 infants (less than 3.5 years) mountain gorillas in the Virunga Massif. Our aim was to conduct the first comprehensive analysis of causes of infant mortality and to correlate histological evidence with antemortem morbidity in infant mountain gorillas. Causes of morbidity and mortality were described, and compared by age, sex, and over time. Trauma was the most common cause of death in infants (56%), followed by respiratory infections and aspiration (13%). Gastrointestinal parasitism (33%), atypical lymphoid hyperplasia (suggestive of infectious disease) (31%), and hepatic capillariasis (25%) were the most significant causes of antemortem morbidity identified post-mortem. Identifying the causes of mortality and morbidity in infants of this critically endangered species will help to inform policy aimed at their protection and guide ante- and post-mortem health monitoring and clinical decision-making in the future.

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.

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

While there are a number of methods available for estimation of body mass in adult nonhuman primates, very few are available for juveniles, despite the potential utility of such estimations in both analyses of fossils and in museum collection based research. Furthermore, because of possible scaling differences, adult based body mass estimation equations may not be appropriate for non-adults. In this study, we present new body mass estimation equations for both adult and immature nonhuman hominoids based on joint and metaphyseal dimensions. Articular breadths of the proximal and distal femur, distal humerus and tibial plateau, and metaphyseal breadths of the distal femur and humerus were collected on a reference sample of 159 wild Pan , Gorilla , Pongo , Hylobates , and Symphalangus specimens of known body mass from museum and research collections. Scaling of dimensions with body weight was assessed in both the adult and the ontogenetic sample at several taxonomic levels using reduced major axis regression, followed by regression of each dimension against body mass to generate body mass estimation equations. Joint dimensions were found to be good predictors of body mass in both adult and immature hominoids, with percent prediction errors of 10–20%. However, subtle scaling differences between taxa impacted body mass estimation, suggesting that phylogeny and locomotor effects should be considered when selecting reference samples. Unlike patterns of joint growth in humans, there was little conclusive evidence for consistently larger joints relative to body mass in the non-adult sample. Metaphyseal breadths were strong predictors of body mass and, with some exceptions, gave more precise body mass estimates for non-adults than epiphyseal breadths.

The robust masticatory system of mountain gorillas is thought to have evolved for the comminution of tough vegetation, yet, compared to other primates, the toughness of the mountain gorilla diet is unremarkable. This may be a result of low plant toughness in the mountain gorilla environment or of mountain gorillas feeding selectively on low-toughness foods. The goal of this paper is to determine how the toughness of the mountain gorilla diet varies across their habitat, which spans a large altitudinal range, and whether there is a relationship between toughness and food selection by mountain gorillas. We collected data on the following variables to determine whether, and if so how, they change with altitude: leaf toughness of two plant species consumed by mountain gorillas, at every 100 m increase in altitude (2,600-3,700 m); toughness of consumed foods comprising over 85% of the gorilla diet across five vegetation zones; and toughness of unconsumed/infrequently consumed plant parts of those foods. Although leaf toughness increased with altitude, the toughness of the gorilla diet remained similar. There was a negative relationship between toughness and consumption frequency, and toughness was a better predictor of consumption frequency than plant frequency, biomass, and density. Consumed plant parts were less tough than unconsumed/infrequently consumed parts and toughness of the latter increased with altitude. Although it is unclear whether gorillas select food based on toughness or use toughness as a sensory cue to impart other plant properties (e.g., macronutrients, chemicals), our results that gorillas maintain a consistent low-toughness dietary profile across altitude, despite toughness increasing with altitude, suggest that the robust gorilla masticatory apparatus evolved for repetitive mastication of foods that are not high in toughness.

Objectives: Ecological factors have a dramatic effect on tooth wear in primates, although it remains unclear how individual age contributes to functional crown morphology. The aim of this study is to determine how age and individual diet are related to tooth wear in wild mountain gorillas (Gorilla beringei beringei) from Volcanoes National Park, Rwanda. Material and Methods: We calculated the percent of dentine exposure (PDE) for all permanent molars (M1–M3) of known-age mountain gorillas (N = 23), to test whether PDE varied with age using regression analysis. For each molar position, we also performed stepwise multiple linear regression to test the effects of age and percentage of time spent feeding on different food categories on PDE, for individuals subject to long-term observational studies by the Dian Fossey Gorilla Fund International's Karisoke Research Center. Results: PDE increased significantly with age for both sexes in all molars. Moreover, a significant effect of gritty plant root consumption on PDE was found among individuals. Our results support prior reports indicating reduced tooth wear in mountain gorillas compared to western gorillas, and compared to other known-aged samples of primate taxa from forest and savanna habitats. Discussion: Our findings corroborate that mountain gorillas present very low molar wear, and support the hypothesis that age and the consumption of particular food types, namely roots, are significant determinants of tooth wear variation in mountain gorillas. Future research should characterize the mineral composition of the soil in the Virunga habitat, to test the hypothesis that the physical and abrasive properties of gritty foods such as roots influence intra- and interspecific patterns of tooth wear. Grant sponsor: National Science Foundation; Grant numbers: BCS 0852866, 0964944; Grant sponsors: The Leakey Foundation; National Geographic Society’s Committee for Exploration and Research; the Center and Institute Facilitating Fund of The George Washington University; the 2010 Max Planck Research Award endowed by the German Federal Ministry of Education and Research to the Max Planck Society; Alexander von Humboldt Foundation.

Amyloid beta (Aβ) and tau pathology have been described in the brains of captive aged great apes, but the natural progression of these age-related pathologies from wild great apes, including the gorilla, is unknown. In our previous study of Western lowland gorillas (Gorilla gorilla gorilla) who were housed in American Zoos and Aquariums-accredited facilities, we found an age-related increase in Aβ-positive plaques and vasculature, tau-positive astrocytes, oligodendrocyte coiled bodies, and neuritic clusters in the neocortex as well as hippocampus in older animals. Here, we demonstrate that aged wild mountain gorillas (Gorilla beringei beringei), who spent their entire lives in their natural habitat, also display an age-related increase in amyloid precursor protein (APP) and/or Aβ-immunoreactive blood vessels and plaques, but very limited tau pathology, in the frontal cortex. These results indicate that Aβ and tau lesions are age-related events that occur in the brain of gorillas living in captivity and in the wild.

Infectious diseases pose one of the most significant threats to the survival of great apes in the wild. The critically endangered mountain gorilla (Gorilla beringei beringei) is at high risk for contracting human pathogens because approximately 60% of the population is habituated to humans to support a thriving ecotourism program. Disease surveillance for human and non-human primate pathogens is important for population health and management of protected primate species. Here, we evaluate discarded plants from mountain gorillas and sympatric golden monkeys (Cercopithecus mitis kandti), as a novel biological sample to detect viruses that are shed orally. Discarded plant samples were tested for the presence of mammalian-specific genetic material and two ubiquitous DNA and RNA primate viruses, herpesviruses, and simian foamy virus. We collected discarded plant samples from 383 wild human-habituated mountain gorillas and from 18 habituated golden monkeys. Mammalian-specific genetic material was recovered from all plant species and portions of plant bitten or chewed by gorillas and golden monkeys. Gorilla herpesviral DNA was most consistently recovered from plants in which leafy portions were eaten by gorillas. Simian foamy virus nucleic acid was recovered from plants discarded by golden monkeys, indicating that it is also possible to detect RNA viruses from bitten or chewed plants. Our findings show that discarded plants are a useful non-invasive sampling method for detection of viruses that are shed orally in mountain gorillas, sympatric golden monkeys, and potentially other species. This method of collecting specimens from discarded plants is a new non-invasive sampling protocol that can be combined with collection of feces and urine to evaluate the most common routes of viral shedding in wild primates. Am. J. Primatol. 78:1222-1234, 2016. © 2016 Wiley Periodicals, Inc.

SUMMARYAnoplocephalid tapeworms of the genus Bertiella Stiles and Hassall, 1902 and Anoplocephala Blanchard, 1848, found in the Asian, African and American non-human primates are presumed to sporadic ape-to-man transmissions. Variable nuclear (5.8S-ITS2; 28S rRNA) and mitochondrial genes (cox1; nad1) of isolates of anoplocephalids originating from different primates (Callicebus oenanthe, Gorilla beringei, Gorilla gorilla, Pan troglodytes and Pongo abelii) and humans from various regions (South America, Africa, South-East Asia) were sequenced. In most analyses, Bertiella formed a monophyletic group within the subfamily Anoplocephalinae, however, the 28S rRNA sequence-based analysis indicated paraphyletic relationship between Bertiella from primates and Australian marsupials and rodents, which should thus be regarded as different taxa. Moreover, isolate determined as Anoplocephala cf. gorillae from mountain gorilla clustered within the Bertiella clade from primates. This either indicates that A. gorillae deserves to be included into the genus Bertiella, or, that an unknown Bertiella species infects also mountain gorillas. The analyses allowed the genetic differentiation of the isolates, albeit with no obvious geographical or host-related patterns. The unexpected genetic diversity of the isolates studied suggests the existence of several Bertiella species in primates and human and calls for revision of the whole group, based both on molecular and morphological data.

Sexually transmitted diseases (STDs) can persist endemically, are known to cause sterility and infant mortality in humans, and could have similar impacts in wildlife populations. African apes (i.e., chimpanzees, bonobos, and to a lesser extent gorillas) show multi-male mating behavior that could offer opportunities for STD transmission, yet little is known about the prevalence and impact of STDs in this endangered primate group. We used serology and PCR-based detection methods to screen biological samples from wild and orphaned eastern chimpanzees and gorillas (N = 172 individuals, including adults, and juveniles) for four classes of pathogens that either commonly cause human STDs or were previously detected in captive apes: trichomonads, Chlamydia spp., Treponema pallidum (syphilis and yaws), and papillomaviruses. Based on results from prior modeling and comparative research, we expected STD prevalence to be highest in females versus males and in sexually mature versus immature individuals. All samples were negative for Chlamydia, Treponema pallidum, and papillomaviruses; however, a high percentage of wild chimpanzee urine and fecal samples showed evidence of trichomonads (protozoa). Analysis revealed that females were more likely than males to have positive urine-but not fecal-samples; however, there was no evidence of age (sexual maturity) differences in infection status. Sequence analysis of chimpanzee trichomonad samples revealed a close relationship to previously described trichomonads within the genus Tetratrichomonas. Phylogenetic comparisons to archived sequences from multiple vertebrate hosts suggests that many of the chimpanzee parasites from our study are likely transmitted via fecal-oral contact, but the transmission of some Tetratrichomonas sequence-types remains unknown and could include sexual contact. Our work emphasizes that only a fraction of infectious agents affecting wild apes are presently known to science, and that further work on great ape STDs could offer insights for the management of endangered great apes and for understanding human STD origins.

The genetic relatedness of mountain gorillas and humans has led to concerns about interspecies transmission of infectious agents. Human-to-gorilla transmission may explain human metapneumovirus in 2 wild mountain gorillas that died during a respiratory disease outbreak in Rwanda in 2009. Surveillance is needed to ensure survival of these critically endangered animals.

Background Infectious diseases represent the greatest threats to endangered species, and transmission from humans to wildlife under increased anthropogenic pressure has been always stated as a major risk of habituation. Aims To evaluate the impact of close contact with humans on the occurrence of potentially zoonotic protists in great apes, one hundred mountain gorillas (Gorilla beringei beringei) from seven groups habituated either for tourism or for research in Volcanoes National Park, Rwanda were screened for the presence of microsporidia, Cryptosporidium spp. and Giardia spp. using molecular diagnostics. Results The most frequently detected parasites were Enterocytozoon bieneusi found in 18 samples (including genotype EbpA, D, C, gorilla 2 and five novel genotypes gorilla 4-8) and Encephalitozoon cuniculi with genotype II being more prevalent (10 cases) compared to genotype I (1 case). Cryptosporidium muris (2 cases) and C. meleagridis (2 cases) were documented in great apes for the first time. Cryptosporidium sp. infections were identified only in research groups and occurrence of E. cuniculi in research groups was significantly higher in comparison to tourist groups. No difference in prevalence of E. bieneusi was observed between research and tourist groups. Conclusion Although our data showed the presence and diversity of important opportunistic protists in Volcanoes gorillas, the source and the routes of the circulation remain unknown. Repeated individual sampling, broad sampling of other hosts sharing the habitat with gorillas and quantification of studied protists would be necessary to acquire more complex data.

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.

Behavioral studies indicate that adult mountain gorillas (Gorilla beringei) are the most terrestrial of all nonhuman hominoids, but that infant mountain gorillas are much more arboreal. Here we examine ontogenetic changes in diaphyseal strength and length of the femur, tibia, humerus, radius, and ulna in 30 Virunga mountain gorillas, including 18 immature specimens and 12 adults. Comparisons are also made with 14 adult western lowland gorillas (Gorilla gorilla gorilla), which are known to be more arboreal than adult mountain gorillas. Infant mountain gorillas have significantly stronger forelimbs relative to hind limbs than older juveniles and adults, but are nonsignificantly different from western lowland gorilla adults. The change in inter-limb strength proportions is abrupt at about two years of age, corresponding to the documented transition to committed terrestrial quadrupedalism in mountain gorillas. The one exception is the ulna, which shows a gradual increase in strength relative to the radius and other long bones during development, possibly corresponding to the gradual adoption of stereotypical fully pronated knuckle-walking in older juvenile gorillas. Inter-limb bone length proportions show a contrasting developmental pattern, with hind limb/forelimb length declining rapidly from birth to five months of age, and then showing no consistent change through adulthood. The very early change in length proportions, prior to significant independent locomotion, may be related to the need for relatively long forelimbs for climbing in a large-bodied hominoid. Virunga mountain gorilla older juveniles and adults have equal or longer forelimb relative to hind limb bones than western lowland adults. These findings indicate that both ontogenetically and among closely related species of Gorilla, long bone strength proportions better reflect actual locomotor behavior than bone length proportions.

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.

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.

Introduction Modern conservation efforts are associated with the use of multidisciplinary approaches to resolve biological and socioeconomic issues. Such conservation efforts include veterinary medicine. However, veterinary participation from inception to completion on conservation projects is frequently far belowits potential (Karesh & Cook, 1995). The fact that veterinarians are trained and actively involved with population, environmental, and epidemiological approaches to medical management of domestic and captive wildlife is often overlooked in wild populations. Since its discovery, the mountain gorilla ( Gorilla gorilla beringei ) has been under many pressures, including habitat encroachment, direct poaching, and trauma from snares set for duiker and bushbuck. Recently, direct and indirect consequences of war, as well as increasing levels of ecotourism (70% of the gorilla population is habituated to humans) with their potential for the introduction of human pathogens to the gorillas, have emerged as significant threats. The intrusion of poachers, soldiers, and domestic animals in fragmented patches facilitates the influx of new pathogens. These factors, combined with the limited area available to the animals, have reduced the ability of wild gorillas to avoid contact with humans. The situation will require increasing veterinary input to help secure the future of the mountain gorillas. Disease management becomes even more important in light of the small size of the mountain gorilla population. With less than 620 animals in two separate populations, the survival of individual gorillas, especially females, becomes a priority, not only to minimize the risk of loss of the entire population in one catastrophic event but also for the maintenance of genetic diversity (Hill, 1999).

Mountain gorillas are an endangered great ape subspecies and a prominent focus for conservation, yet we know little about their genomic diversity and evolutionary past. We sequenced whole genomes from multiple wild individuals and compared the genomes of all four Gorilla subspecies. We found that the two eastern subspecies have experienced a prolonged population decline over the past 100,000 years, resulting in very low genetic diversity and an increased overall burden of deleterious variation. A further recent decline in the mountain gorilla population has led to extensive inbreeding, such that individuals are typically homozygous at 34% of their sequence, leading to the purging of severely deleterious recessive mutations from the population. We discuss the causes of their decline and the consequences for their future survival. © 2015, American Association for the Advancement of Science. All rights reserved., Supported by Royal Society grant RG130105 (A.S.), Wellcome Trust grants 098051 (Q.A., Y.C., V.N., L.P., M.A.Q., M.S., C.T.-S., Y.X., B.Y.) and 099769/Z/12/Z (V.N.), NIH grant HG002385 (E.E.E.), a European Research Council Starting Grant (260372), and Ministerio de Ciencia e Innovacion grant BFU2011-28549 (T.M.-B.).