Continued ecosystem changes create a dynamic ensemble of threats for wildlife species of conservation concern, including emergence of novel pathogens, a prominent risk amongst isolated populations with lowered resilience. Success in the conservation of mountain gorillas (Gorilla beringei beringei) is owed to intensive stewardship over the last three decades, with ongoing management required in the face of continued global change. Recently, increased clinical disease occurrence is reported amongst the only two extant mountain gorilla populations, with symptoms typical of strongylid nematode infections. Using historic biobanked faecal samples, we assessed changes in the strongylid nematode communities of both isolated mountain gorilla populations between two decades, employing high-throughput sequencing to describe their genetic diversity and explore their relevance to clinical case emergence. We applied ITS-2 metabarcoding within the Illumina MiSeq platform for strain-level identification. We uncover major temporal variability of strongylid communities in the region with the highest disease occurrence, revealing that dominance of pathogenic Hyostrongylus has emerged within this region within the last two decades. This coincides with considerable changes in gorilla social structure in this region since 2007, following continuous population growth but limited ability for spatial expansion. The recovery of mountain gorillas provides a valuable lesson to conservation science yet highlights how ongoing growth of any island populations requires vigilant management to ensure resilience. Emerging threats, such as novel diseases, must be carefully considered within these management plans, with biobanking and long-term monitoring a vital conservation tool for preventing biodiversity loss.

There are no published data on the occurrence of neoplasia in wild great apes of any species. The aim of this study was to utilize postmortem and histopathology reports collected from wild human-habituated mountain gorillas (Gorilla beringei beringei) and Grauer's gorillas (Gorilla beringei graueri) to determine both the incidence and types of spontaneous neoplasms and proliferative lesions that occur in these species. Pathology records of 194 mountain gorillas and 12 Grauer's gorillas necropsied from 1985 to 2020 were examined for all cases of neoplasia or hyperplastic/proliferative disease. Slides and/or scanned images were reviewed to confirm morphologic diagnoses. Data were collected on comorbidities that may have contributed to neoplastic/proliferative transformation. A total of nine malignant neoplasms were identified: large cell anaplastic B-cell lymphoma, gastric adenocarcinoma (two cases), gastric carcinoid, oral mucocutaneous malignant melanoma, gastric carcinoma in situ (two cases), squamous cell carcinoma of the lip, and renal adenocarcinoma. Benign lesions included pheochromocytoma, adrenocortical adenoma (two cases), parathyroid adenoma, mandibular fibroma with gingival hyperplasia, and uterine hemangioma. Proliferative gastritis was commonly identified secondary to gastrointestinal parasitism (n = 35); chronic inflammation from nematodiasis may have led to neoplastic transformation of hyperplastic mucosal epithelium. Other hyperplastic lesions included nodular hyperplasia of the adrenal cortex (n = 9), adrenal medulla (n = 7) and thyroid glands (n = 3), pulmonary reactive lymphoid hyperplasia in infants and juveniles (n = 16), as well as nodular splenic siderofibrosis (n = 5) that may be associated with parasite migration. These findings demonstrate that free-ranging mountain and Grauer's gorillas in a natural environment develop neoplasia and proliferative disease.

Cestodes of the family Anoplocephalidae parasitize a wide range of usually herbivorous hosts including e.g. rodents, ungulates, primates, elephants and hyraxes. While in some hosts, the epidemiology of the infection is well studied, information is lacking in others. In this study of mountain gorillas in the Virunga Massif, an extensive sample set comprising adult cestodes collected via necropsies, proglottids shed in feces, and finally, fecal samples from both night nests and identified individuals were analysed. Anoplocephala gorillae was the dominant cestode species detected in night nest samples and individually known gorillas, of which only 1 individual hosted a Bertiella sp. It was shown that the 2 species can be distinguished through microscopy based on egg morphology and polymerase chain reaction (PCR) assays for diagnostics of both species were provided. Sequences of mitochondrial (cox 1) and nuclear (ITS1, 18S rDNA, 28S rDNA) markers were used to evaluate the phylogenetic position of the 2 cestodes detected in mountain gorillas. Both types of fecal samples, from night nests and from identified individuals, provided comparable information about the prevalence of anoplocephalid cestodes, although the analysis of samples collected from identified gorilla individuals showed significant intra-individual fluctuation of A. gorillae egg shedding within a short period. Therefore, multiple samples should be examined to obtain reliable data for wildlife health management programmes, especially when application of anthelmintic treatment is considered. However, while A. gorillae is apparently a common symbiont of mountain gorillas, it does not seem to impair the health of its host.

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.

Mountain gorillas are particularly inbred compared to other gorillas and even the most inbred human populations. As mountain gorilla skeletal material accumulated during the 1970s, researchers noted their pronounced facial asymmetry and hypothesized that it reflects a population-wide chewing side preference. However, asymmetry has also been linked to environmental and genetic stress in experimental models. Here, we examine facial asymmetry in 114 crania from three Gorilla subspecies using 3D geometric morphometrics. We measure fluctuating asymmetry (FA), defined as random deviations from perfect symmetry, and population-specific patterns of directional asymmetry (DA). Mountain gorillas, with a current population size of about 1000 individuals, have the highest degree of facial FA (explaining 17% of total facial shape variation), followed by Grauer gorillas (9%) and western lowland gorillas (6%), despite the latter experiencing the greatest ecological and dietary variability. DA, while significant in all three taxa, explains relatively less shape variation than FA does. Facial asymmetry correlates neither with tooth wear asymmetry nor increases with age in a mountain gorilla subsample, undermining the hypothesis that facial asymmetry is driven by chewing side preference. An examination of temporal trends shows that stress-induced developmental instability has increased over the last 100 years in these endangered apes.

Infectious diseases have the potential to extirpate populations of great apes. As the interface between humans and great apes expands, zoonoses pose an increasingly severe threat to already endangered great ape populations. Despite recognition of the threat posed by human pathogens to great apes, health monitoring is only conducted for a small fraction of the world's wild great apes (and mostly those that are habituated) meaning that outbreaks of disease often go unrecognized and therefore unmitigated. This lack of surveillance (even in sites where capacity to conduct surveillance is present) is the most significant limiting factor in our ability to quickly detect and respond to emerging infectious diseases in great apes when they first appear. Accordingly, we must create a surveillance system that links disease outbreaks in humans and great apes in time and space, and enables veterinarians, clinicians, conservation managers, national decision makers, and the global health community to respond quickly to these events. Here, we review existing great ape health surveillance programs in African range habitats to identify successes, gaps, and challenges. We use these findings to argue that standardization of surveillance across sites and geographic scales, that monitors primate health in real-time and generates early warnings of disease outbreaks, is an efficient, low-cost step to conserve great ape populations. Such a surveillance program, which we call "Great Ape Health Watch" would lead to long-term improvements in outbreak preparedness, prevention, detection, and response, while generating valuable data for epidemiological research and sustainable conservation planning. Standardized monitoring of great apes would also make it easier to integrate with human surveillance activities. This approach would empower local stakeholders to link wildlife and human health, allowing for near real-time, bidirectional surveillance at the great ape-human interface.

A 30-year-old free-ranging female mountain gorilla (Gorilla beringei beringei) developed a perioral mass that was surgically debulked and diagnosed as malignant melanoma. After tumor recurrence, a canine melanoma vaccine was administered. However, the gorilla died shortly thereafter, and metastases to lymph nodes, lung, liver, and kidney were found post-mortem.

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 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.

Monitoring population size and growth over time is vital for the conservation of endangered species. Mountain gorillas Gorilla beringei beringei remain in two small populations that span the borders of the Democratic Republic of Congo, Rwanda and Uganda. Each population contains two subpopulations that receive differing levels of protection: the monitored groups are visited daily by park staff and researchers and can be counted by sight, whereas the number and growth rate of unmonitored gorillas must be estimated indirectly. Here, we re-analyze published data from a survey in 2010 combined with new results from a survey conducted during two sampling occasions in 2015 and 2016 to estimate mountain gorilla abundance and growth in the Virunga Massif between 2010 and 2016. Using genetic analysis of non-invasively collected samples and two capture-mark-recapture estimates, we estimated that the 186 detected genotypes represented 221 (95% credible interval: 204-243) to 251 (205-340) unmonitored gorillas in 2016. Together with the 418 monitored gorillas, the overall population of the Virunga Massif thus reached 639 (622-661) to 669 (623-758) individuals. We estimated the growth of the entire Virunga Massif population at about 3% per year, but determined that the growth of the monitored gorillas (4.4%) mainly drove that increase. In contrast, the trend of the unmonitored subpopulation could not be determined with confidence because both models provided 95% CI that encompassed zero: 0.5% per year (-0.7% to +1.7%) and 1.1% (-2.7% to +4.4%). While the overall growth rate represents a rare success story for primate conservation, our results highlight the need for greater protection of unmonitored gorillas.

Between December 2002 and September 2017, 125 anesthetic procedures involving free-living and orphaned captive mountain gorillas (Gorilla beringei beringei) were performed in the Virunga Massif and Bwindi Impenetrable Forest in East-Central Africa. Of these 125 immobilizations, 114 records were complete enough for inclusion into this study. Anesthetic and physiologic data from these 114 cases were analyzed, of which 57 used medetomidine-ketamine and 57 used dexmedetomidine-ketamine administered intramuscularly. With the use of estimated weights, the mean induction dosage (mg/kg +/- SD) for medetomidine was 0.033 +/- 0.003 (n = 42), for dexmedetomidine 0.018 +/- 0.005 (n = 53), and for ketamine 3.66 +/- 0.95 (n = 95). Mean time from injection of induction dose to recumbency was 6.8 +/- 3.1 min (n = 74). Atipamezole was administered intramuscularly to reverse anesthesia. First signs of recovery occurred at 5.0 +/- 4.0 min, and full recovery was 19.0 +/- 17.0 min after administration of the reversal agent. No significant differences in physiologic parameters or anesthetic time variables were noted between healthy and unhealthy individuals. Mean heart rate was 72.0 +/- 17.6 beats/min (n = 83) and mean oxygen saturation was 96.5% +/- 4.2 (n = 62). Mean respiratory rate was 27 +/- 9 breaths/min (n = 84) and mean body temperature 36.6 degrees C +/- 1.2 (n = 61). The current protocol has several advantages for field use in this species given its quick induction, few observed side effects, and ability to reverse so that the animal can return more quickly to its social group.

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.

Mutations in the Plasmodium falciparumk13 (Pfk13) gene are linked to delayed parasite clearance in response to artemisinin-based combination therapies (ACTs) in Southeast Asia. To explore the evolutionary rate and constraints acting on this gene, k13 orthologs from species sharing a recent common ancestor with P. falciparum and Plasmodium vivax were analyzed. These comparative studies were followed by genetic polymorphism analyses within P. falciparum using 982 complete Pfk13 sequences from public databases and new data obtained by next-generation sequencing from African and Haitian isolates. Although k13 orthologs evolve at heterogeneous rates, the gene was conserved across the genus, with only synonymous substitutions being found at residues where mutations linked to the delayed parasite clearance phenotype have been reported. This suggests that those residues were under constraint from undergoing nonsynonymous changes during evolution of the genus. No fixed nonsynonymous differences were found between Pfk13 and its orthologs in closely related species found in African apes. This indicates that all nonsynonymous substitutions currently found in Pfk13 are younger than the time of divergence between P. falciparum and its closely related species. At the population level, no mutations linked to delayed parasite clearance were found in our samples from Africa and Haiti. However, there is a high number of single Pfk13 mutations segregating in P. falciparum populations, and two predominant alleles are distributed worldwide. This pattern is discussed in terms of how changes in the efficacy of natural selection, affected by population expansion, may have allowed for the emergence of mutations tolerant to ACTs.

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.

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 King Penguin (Aptenodytes patagonicus) is a pelagic seabird that breeds on Subantarctic islands and is considered a rare vagrant in South Africa. From 2001 to 2017, six King Penguins were rescued along the South African coast and admitted into rehabilitation centers. These and previous records of King Penguins were obtained near the country’s major ports, which suggests that some of these birds may have been ship-assisted. One of the King Penguins evaluated in this study died shortly after being admitted to the rehabilitation center due to extensive hemorrhage caused by a long-line fishing hook, and another had a beak wound consistent with fishing hook injury. Three King Penguins were infected with the tick-borne protozoan Babesia peircei and two died as a result of babesiosis. One King Penguin was diagnosed with an infection by Rickettsia-like organisms. Pox-like lesions, presumably mosquito-borne, developed on the eyelid skin of one penguin. Additionally, one of two King Penguins permanently captive in Cape Town during the same period also presented a lethal case of spirochetosis, which was possibly tick-borne. These novel records of vector-borne pathogens in King Penguins highlight the risk of seabird rehabilitation centers to serve as potential sources of pathogens to vagrant species, while also illustrating the opportunities that these centers provide for pathogen research and surveillance.