1. Conservation success stories, such as the recovery of the isolated populations of mountain gorilla (Gorilla beringei beringei), are increasingly threatened by emerging health challenges. In the Virunga Massif, strongylid-associated gastrointestinal disease has been linked to significant morbidity and mortality of mountain gorillas, posing a critical threat to this population's long-term survival. 2. Using metabarcoding of faecal samples (similar to 65% of the population) and spatial and habitat analyses, we examined the composition and drivers of strongylid nematode communities and their role in clinical disease emergence. 3. We identified Hyostrongylus nematodes, known pathogens in suids, as the primary contributors to gastric lesions observed in necropsied gorillas. Spatial variation in strongylid communities is correlated with environmental gradients, indicating that environmental factors such as climate and vegetation play a significant role in shaping strongylid community composition. Additionally, limited genetic diversity resulting from historical population bottlenecks may negatively impact the health of gorillas affected by parasites. 4. Our findings suggest that the high absolute abundance of pathogenic Hyostrongylus is concentrated in specific high-altitude regions, aligning with observed cases of severe gastritis. 5. Synthesis and applications. These findings highlight an emerging health threat for mountain gorillas, with implications for other isolated wildlife populations facing similar ecological and evolutionary pressures. The study calls for continued monitoring of parasitic diseases in wildlife populations, especially those in fragmented habitats with limited capacity for expansion, to mitigate potential risks to their conservation.
The number of mountain gorillas (Gorilla beringei beringei) has grown steadily in recent decades thanks to intensive conservation efforts. But as they live in restricted areas, they experience changes in population dynamics and pathogen epidemiology. These changes have been demonstrated by the emergence of gastrointestinal problems linked to strongylid infections in the Virunga population, highlighting the need to study changes in other parasite infections. We assessed the patterns of Cryptosporidium, Giardia and microsporidia infections in mountain gorillas across the Virunga Massif. We examined 152 faecal samples from 16 gorilla groups collected in 2018 using PCR and qPCR on three genetic markers and detected Cryptosporidium muris (< 1%), Enterocytozoon bieneusi (genotypes-D 14%, CHN-F1 < 1%) and Giardia intestinalis (13%). No significant spatial or sex/age differences were observed in microsporidia and Giardia infections. However, a temporal comparison with previous data suggests changes in the protist communities over time. We conclude that these protists were not impacted by the changes in mountain gorilla population dynamics and did not contribute to the increasing occurrence of severe gastrointestinal problems in Virunga gorillas. These results aid our epidemiological understanding of parasite communities in mountain gorillas, an asset for their ongoing conservation management in the face of newly emerging health challenges.
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.
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.
Strategies to reduce illegal resource collection vary depending on the assumptions made about the underlying drivers of resource use. Interventions to reduce illegal resource use commonly include law enforcement, integrated conservation and development projects, and environmental education. Despite using a mixture of strategies, illegal activities continue to threaten the endangered mountain gorilla (Gorilla beringei beringei) in Volcanoes National Park (VNP), Rwanda. For conservation interventions to work effectively, it is important to understand the drivers of and motivations behind illegal resource use. To assess the drivers of, motivations behind, and deterrents to illegal resource use, we combined interviews of suspected illegal resource users with a larger household survey, indirect questioning (unmatched count technique), and focus groups. Overall, illegal resource use was most common among large households with lower well-being scores. Illegal resource users were more likely to report a problem from living near VNP and tended to be from households whose primary form of income was part-time labor. Although poverty was associated with illegal resource use overall, we found that several illegal resource users came from locally wealthy households and were motivated primarily by profit. Demand for forest products, like wild meat, highlights the structural factors likely behind illegal resource use and warrants further investigation. Because the drivers of illegal resource use varied between households, we find that neither law enforcement nor livelihood projects alone will decrease illegal resource use. Instead, effective conservation interventions require a multipronged approach to address the complex motivations of illegal resource use.
Context Biodiversity monitoring programs provide information on the status and trends in wildlife populations. These trends are unknown for most mammals within African montane forests, which harbour many endemic and threatened species. Camera traps are useful for assessing mammal populations, because they allow for the estimation of species richness, occupancy, and activity patterns. Aims We sought to explore the richness and distribution of small- to large-sized mammals by using occupancy models while accounting for imperfect detection in Volcanoes and Mgahinga Gorilla National Parks, in Rwanda and Uganda. Methods We used camera-trap data collected from 2014 to 2017 by the Tropical Ecology Assessment and Monitoring (TEAM) network and multi-season occupancy models with multispecies data to assess the dynamics of species richness and distribution in the Virunga Massif and the influence of site covariates on species detection probability, occupancy, colonisation and extinction. Key results We identified 17 species from 7047 trap-days, with most of them showing an uneven distributional pattern throughout the park. We found that average species richness per site increased from five to seven species in 2017. Average local colonisation was estimated at 0.13 (s.e. 0.014), but the probability of local extinction was 0.17 (s.e. 0.028) and negatively influenced by distance from the park boundary. Detection probability was highest for medium-sized species. For species distribution, we found that black-fronted duiker, Cephalophus nigrifrons, and bushbuck, Tragelaphus scriptus, declined in distribution but remained widespread in our study area, while all other species showed an increase in distribution over the study period. Conclusions Our approach allowed us to draw inferences on rare species, such as African golden cat, Caracal aurata, by estimating detection probability on the basis of shared covariate information with more common, widespread species. As such, we were able to estimate all occupancy parameters across the terrestrial mammal community. Implications The results of this study on the distribution of terrestrial mammal species can be used by park management to inform optimal ranger patrolling efforts for mitigating threats in areas of high species presence. Additionally, the results can highlight locations of potential human–wildlife conflicts on the basis of species commonly found along the park boundary.
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.
Poaching is a pervasive threat to wildlife, yet quantifying the direct effect of poaching on wildlife is rarely possible because both wildlife and threat data are infrequently collected concurrently. In this study, we used poaching data collected through the Management Information System (MIST) and wildlife camera trap data collected by the Tropical Ecology Assessment and Monitoring (TEAM) network from 2014 to 2017 in Volcanoes National Park, Rwanda. We implemented co-occurrence multi-season occupancy models that accounted for imperfect detection to investigate the effect of poaching on initial occupancy, colonization, and extinction of five mammal species. Specifically, we focused on two species of conservation concern (mountain gorilla [Gorilla beringei beringei] and golden monkey [Cercopithecus mitis kandti]), and three species targeted by poachers (black-fronted duiker [Cephalophus nigrifrons], bushbuck [Tragelaphus scriptus], and African buffalo [Syncerus caffer]). We found that the probability of local extinction was highest in sites with poaching activity for golden monkey and bushbuck. In addition, the probability of initial occupancy for golden monkey was highest in sites without poaching activity. We only found weak evidence of effects of poaching on parameters governing the occupancy dynamics of the other species. All species showed evidence of poaching presence affecting the probability of detection of the wildlife species. This is the first study to our knowledge to combine direct threat observations from ranger-based monitoring data with camera trap wildlife observations to quantify the effect of poaching on wildlife. Given the widespread collection of ranger-based monitoring and camera trap data, our approach is broadly applicable to numerous protected areas and has the potential to significantly improve conservation management. Specifically, the relationship between poaching activity and wildlife population dynamics can be combined with information on the relationship between ranger patrols and poaching activity to develop models useful for making wise decisions about ranger patrol deployment.
When mothers continue to support their offspring beyond infancy, they can influence the fitness of those offspring, the strength of social relationships within their groups, and the life-history traits of their species. Using up to 30 years of demographic data from 58 groups of gorillas in two study sites, this study extends such findings by showing that mothers may also contribute to differences in social organization between closely related species. Female mountain gorillas remained with their sons for significantly longer than western gorillas, which may explain why male philopatry and multimale groups are more common among mountain gorillas. The presence of the putative father and other familiar males did not vary significantly between species, and we found only limited support for the socio-ecological theory that the distribution of adult males is influenced by the distribution of females. Within each gorilla species, variations in those distributions may also reflect the different stages in the typical life cycle of a group. Collectively, our results highlight the potentially far-reaching consequences of maternal support that extends beyond infancy, and they illustrate the opportunity to incorporate additional factors into phylogenetic analyses of variations in social organization, including studies of human evolution.
Using 30 years of demographic data from 15 groups, this study estimates how harem size, female fertility, and offspring survival may contribute to variance in the siring rates of dominant male mountain gorillas throughout the Virunga Volcano Region. As predicted for polygynous species, differences in harem size were the greatest source of variance in the siring rate, whereas differences in female fertility and offspring survival were relatively minor. Harem size was positively correlated with offspring survival, even after removing all known and suspected cases of infanticide, so the correlation does not seem to reflect differences in the ability of males to protect their offspring. Harem size was not significantly correlated with female fertility, which is consistent with the hypothesis that mountain gorillas have minimal feeding competition. Harem size, offspring survival, and siring rates were not significantly correlated with the proportion of dominant tenures that occurred in multimale groups versus one-male groups; even though infanticide is less likely when those tenures end in multimale groups than one-male groups. In contrast with the relatively small contribution of offspring survival to variance in the siring rates of this study, offspring survival is a major source of variance in the male reproductive success of western gorillas, which have greater predation risks and significantly higher rates of infanticide. If differences in offspring protection are less important among male mountain gorillas than western gorillas, then the relative importance of other factors may be greater for mountain gorillas. Thus, our study illustrates how variance in male reproductive success and its components can differ between closely related species.
Infanticide can be a major influence upon the social structure of species in which females maintain long-term associations with males. Previous studies have suggested that female mountain gorillas benefit from residing in multimale groups because infanticide occurs when one-male groups disintegrate after the dominant male dies. Here we measure the impact of infanticide on the reproductive success of female mountain gorillas, and we examine whether their dispersal patterns reflect a strategy to avoid infanticide. Using more than 40 years of data from up to 70% of the entire population, we found that only 1.7% of the infants that were born in the study had died from infanticide during group disintegrations. The rarity of such infanticide mainly reflects a low mortality rate of dominant males in one-male groups, and it does not dispel previous observations that infanticide occurs during group disintegrations. After including infanticide from causes other than group disintegrations, infanticide victims represented up to 5.5% of the offspring born during the study, and they accounted for up to 21% of infant mortality. The overall rates of infanticide were 2-3 times higher in one-male groups than multimale groups, but those differences were not statistically significant. Infant mortality, the length of interbirth intervals, and the age of first reproduction were not significantly different between one-male versus multimale groups, so we found no significant fitness benefits for females to prefer multimale groups. In addition, we found limited evidence that female dispersal patterns reflect a preference for multimale groups. If the strength of selection is modest for females to avoid group disintegrations, than any preference for multimale groups may be slow to evolve. Alternatively, variability in male strength might give some one-male groups a lower infanticide risk than some multimale groups, which could explain why both types of groups remain common.
Monitoring changes in the population dynamics of endangered species is crucial to effective conservation strategies. The mountain gorilla population of the Virunga Massif has been the subject of intensive conservation efforts, research and several censuses over the last 40 years, but the region has also been affected by political instability and war. Here we present results from the 2010 census, which was the first to utilize genetic analyses of fecal samples for the entire population. The genetic analyses improved the accuracy of the population estimate by identifying several instances in which gorillas otherwise would have been undercounted or double-counted. The population was estimated to be 480 individuals; including 349 individuals found in 24 groups that were habituated for research and tourism, 101 individuals found in 12 unhabituated groups, fourteen solitary males, and a correction factor of sixteen for undetected infants. The population has increased by 26% since 2003 (an annual rate of 3.7%) and it has almost doubled since 1981. Nearly all of the increase can be attributed to a relatively higher growth rate in the habituated groups from 2003 to 2010, and in all five of the previous intervals between consecutive censuses. Nonetheless, it would be imprudent to habituate additional groups due to the concomitant risks of disease transmission from humans, behavioral disturbance and potential vulnerability to poaching. The results show that it is possible for conservation efforts to succeed even under difficult conditions, while highlighting the continuing challenges of managing a wild population of both habituated and unhabituated gorillas. (C) 2012 Elsevier Ltd. All rights reserved.
As wildlife populations are declining, conservationists are under increasing pressure to measure the effectiveness of different management strategies. Conventional conservation measures such as law enforcement and community development projects are typically designed to minimize negative human influences upon a species and its ecosystem. In contrast, we define "extreme" conservation as efforts targeted to deliberately increase positive human influences, including veterinary care and close monitoring of individual animals. Here we compare the impact of both conservation approaches upon the population growth rate of the critically endangered Virunga mountain gorillas (Gorilla beringei beringei), which increased by 50% since their nadir in 1981, from approximately 250 to nearly 400 gorillas. Using demographic data from 1967-2008, we show an annual decline of 0.7%±0.059% for unhabituated gorillas that received intensive levels of conventional conservation approaches, versus an increase 4.1%±0.088% for habituated gorillas that also received extreme conservation measures. Each group of habituated gorillas is now continuously guarded by a separate team of field staff during daylight hours and receives veterinary treatment for snares, respiratory disease, and other life-threatening conditions. These results suggest that conventional conservation efforts prevented a severe decline of the overall population, but additional extreme measures were needed to achieve positive growth. Demographic stochasticity and socioecological factors had minimal impact on variability in the growth rates. Veterinary interventions could account for up to 40% of the difference in growth rates between habituated versus unhabituated gorillas, with the remaining difference likely arising from greater protection against poachers. Thus, by increasing protection and facilitating veterinary treatment, the daily monitoring of each habituated group contributed to most of the difference in growth rates. Our results argue for wider consideration of extreme measures and offer a startling view of the enormous resources that may be needed to conserve some endangered species.
The mountain gorillas (Gorilla beringei beringei) of the Virunga Volcanoes Range of Rwanda, Uganda, and the Democratic Republic of Congo are one of the most endangered ape populations in the world. Following a dramatic decline during the 1960s, and relative stability in the 1970s, the population steadily increased during the 1980s. Due to political instability and war, a complete census had not been conducted since 1989. Here we compare the results of a complete census using the 'sweep method' conducted in 2003 with those from a monitoring program, to estimate the size and distribution of the gorilla population. A total of 360 gorillas were counted from census measurements and known habituated groups. Based on quantitative assessments of the census accuracy, we calculated that an additional 20 gorillas were not counted, leading to an estimated population of 380 individuals, and a 1.15% annual growth rate since 1989. The Ranger Based Monitoring programme yielded similar results. The encouraging results must be viewed with caution, however, because the growth was concentrated almost entirely in one section of the Virungas. Additionally, the distribution of gorilla groups was negatively correlated with the frequency of human disturbances, which highlights the need to continue strengthening conservation efforts.ResumeLes gorilles de montagne Gorilla gorilla beringei de l'aire de repartition des Volcans Virunga, au Rwanda, en Ouganda et en Republique Democratique du Congo, sont une des populations de grands singes les plus menacees du monde. Apres un declin dramatique dans le courant des annees 1960, et une stabilite relative dans les annees 1970, la population s'est fermement reconstituee au cours des annees 1980. Mais en raison de l'instabilite politique et de la guerre, il n'y avait plus eu de recensement total depuis 1989. Nous comparons ici les resultats d'un recensement complet effectue en 2003 par la methode du balayage topologique (sweep method) avec ceux d'un programme de suivi, afin d'estimer la taille et la distribution de la population de gorilles. Nous avons denombre un total de 360 gorilles en reprenant les chiffres du recensement et ceux des groupes habitues connus. En nous basant sur l'evaluation quantitative de la precision du recensement, nous avons calcule que 20 gorilles supplementaires n'avaient pas ete comptes, ce qui porte l'estimation a 380 individus et signifie un taux de croissance annuel de 1,15% depuis 1989. Le Programme de Suivi base sur les gardes a obtenu des resultats comparables. Pourtant, ces resultats encourageants doivent etre interpretes avec prudence etant donne que la croissance s'est presque entierement concentree sur une seule section des Virunga. De plus, la distribution des groupes de gorilles etait negativement liee a la frequence des perturbations humaines, ce qui souligne la necessite de poursuivre le renforcement des mesures de conservation.