Social and ecological factors alter stress physiology of Virunga mountain gorillas (Gorilla beringei beringei)

Living in a rapidly changing environment can alter stress physiology at the population level, with negative impacts on health, reproductive rates, and mortality that may ultimately result in species decline. Small, isolated animal populations where genetic diversity is low are at particular risks, such as endangered Virunga mountain gorillas (Gorilla beringei beringei). Along with climate change‐associated environmental shifts that are affecting the entire population, subpopulations of the Virunga gorillas have recently experienced extreme changes in their social environment. As the growing population moves closer to the forest's carrying capacity, the gorillas are coping with rising population density, increased frequencies of interactions between social units, and changing habitat use (e.g., more overlapping home ranges and routine ranging at higher elevations). Using noninvasive monitoring of fecal glucocorticoid metabolites (FGM) on 115 habituated Virunga gorillas, we investigated how social and ecological variation are related to baseline FGM levels, to better understand the adaptive capacity of mountain gorillas and monitor potential physiological indicators of population decline risks. Generalized linear mixed models revealed elevated mean monthly baseline FGM levels in months with higher rainfall and higher mean maximum and minimum temperature, suggesting that Virunga gorillas might be sensitive to predicted warming and rainfall trends involving longer, warmer dry seasons and more concentrated and extreme rainfall occurrences. Exclusive use of smaller home range areas was linked to elevated baseline FGM levels, which may reflect reduced feeding efficiency and increased travel efforts to actively avoid neighboring groups. The potential for additive effects of stress‐inducing factors could have short‐ and long‐term impacts on the reproduction, health, and ultimately survival of the Virunga gorilla population. The ongoing effects of environmental changes and population dynamics must be closely monitored and used to develop effective long‐term conservation strategies that can help address these risk factors.     

Censusing the mountain gorillas in the Virunga Volcanoes: complete sweep method versus monitoring

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.     

Ranger Based Monitoring in the Virunga–Bwindi Region of East-Central Africa: A Simple Data Collection Tool for Park Management

Effective management of protected areas is dependent on information on the illegal and legal use of the habitat by people, the ecological and behavioural needs of key species, and trends in resource availability and ecological processes. The International Gorilla Conservation Programme working with the protected area authorities in Rwanda, Uganda and the Democratic Republic of Congo has developed a ranger based monitoring system, using basic protocols for data collection that guide protected area staff in park management. This programme is a key management tool for the three park authorities responsible for the conservation of the mountain gorilla (Gorilla beringei beringei) in the Virunga and Bwindi forest blocks. The programme was initiated in 1997 and has enabled the gathering of extensive information on illegal activities, key species of fauna and flora, and habituated and unhabituated groups of gorillas. Ranger based monitoring is a simple and cost effective tool that can be sustained in the parks in the Virunga–Bwindi region with limited external support. It provides park managers with information that prompts appropriate responses to threats to the ecosystem. For example information on the distribution of illegal activities determines targeted patrol coverage to address specific threats. The bottom-up approach of ranger based monitoring includes a strong capacity building component and empowers field staff in park management activities.     

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

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

Genetic identification of elusive animals: re-evaluating tracking and nesting data for wild western gorillas

Western gorillas Gorilla gorilla have been exceedingly difficult to habituate to the presence of human observers. Nevertheless, researchers have amassed a wealth of information on population densities and group structure for this ape species by locating and counting the sleeping nests of wild individuals. Such nest-count studies have suggested that western gorilla groups often have multiple silverbacks and these multimale groups occasionally divide into smaller subgroups. However, observational data from forest clearing sites and from a few recently habituated western gorilla groups show no evidence of multimale family groups or of subgrouping. This discrepancy underscores a long-standing question in ape research: How accurately do nesting sites reflect true group compositions? We evaluated these indirect measures of group composition by using DNA from faeces and hair to genetically identify individual gorillas at nesting sites. Samples were collected from unhabituated wild western gorillas ranging near Mondika Research Center in the Central African Republic and Republic of Congo. DNA extracted from these samples was genotyped at up to 10 microsatellite loci and one X–Y homologous locus for sex identification. Individuals were then identified at nesting sites by their unique multilocus genotypes, thus providing a 'molecular census' of individual gorillas. Results confirm that western gorillas often build more than one nest at a nesting site and, thus, nest counts can be highly inaccurate indicators of group size and composition. Indeed, we found that nest counts can overestimate group size by as much as 40%, indicating that true gorilla population numbers are probably lower than those reported from census surveys. This study demonstrates how genetic analysis can be a valuable tool for studying and conserving elusive, endangered animals.     

Simulation of the population dynamics and social structure of the Virunga mountain gorillas

An agent-based model was developed to simulate the growth rate, age structure, and social system of the endangered mountain gorillas (Gorilla beringei beringei) in the Virunga Volcanoes region. The model was used to compare two types of data: 1) estimates of the overall population size, age structure, and social structure, as measured by six censuses of the entire region that were conducted in 1971-2000; and 2) information about birth rates, mortality rates, dispersal patterns, and other life history events, as measured from three to five habituated research groups since 1967. On the basis of the research-group data, the "base simulation" predicted a higher growth rate than that observed from the census data (3% vs. 1%). This was as expected, because the research groups have indeed grown faster than the overall population. Additional simulations suggested that the research groups primarily have a lower mortality rate, rather than higher birth rates, compared to the overall population. Predictions from the base simulation generally fell within the range of census values for the average group size, the percentage of multimale groups, and the distribution of females among groups. However, other discrepancies predicted from the research-group data were a higher percentage of adult males than observed, an overestimation of the number of multimale groups with more than two silverbacks, and an overestimated number of groups with only two or three members. Possible causes for such discrepancies include inaccuracies in the census techniques used, and/or limitations with the long-term demographic data set obtained from only a few research groups of a long-lived species. In particular, estimates of mortality and male dispersal obtained from the research groups may not be representative of the entire population. Our final simulation addressed these discrepancies, and provided a better basis for further studies on the complex relationships among individual life history events, group composition, population age structure, and growth rate patterns.     

Ape conservation physiology: fecal glucocorticoid responses in wild Pongo pygmaeus morio following human visitation

Nature-based tourism can generate important revenue to support conservation of biodiversity. However, constant exposure to tourists and subsequent chronic activation of stress responses can produce pathological effects, including impaired cognition, growth, reproduction, and immunity in the same animals we are interested in protecting. Utilizing fecal samples (N = 53) from 2 wild habituated orangutans (Pongo pygmaeus morio) (in addition to 26 fecal samples from 4 wild unhabituated orangutans) in the Lower Kinabatangan Wildlife Sanctuary of Sabah, Malaysian Borneo, we predicted that i) fecal glucocorticoid metabolite concentrations would be elevated on the day after tourist visitation (indicative of normal stress response to exposure to tourists on the previous day) compared to samples taken before or during tourist visitation in wild, habituated orangutans, and ii) that samples collected from habituated animals would have lower fecal glucocorticoid metabolites than unhabituated animals not used for tourism. Among the habituated animals used for tourism, fecal glucocorticoid metabolite levels were significantly elevated in samples collected the day after tourist visitation (indicative of elevated cortisol production on the previous day during tourist visitation). Fecal glucocorticoid metabolite levels were also lower in the habituated animals compared to their age-matched unhabituated counterparts. We conclude that the habituated animals used for this singular ecotourism project are not chronically stressed, unlike other species/populations with documented permanent alterations in stress responses. Animal temperament, species, the presence of coping/escape mechanisms, social confounders, and variation in amount of tourism may explain differences among previous experiments. Acute alterations in glucocorticoid measures in wildlife exposed to tourism must be interpreted conservatively. While permanently altered stress responses can be detrimental, preliminary results in these wild habituated orangutans suggest that low levels of predictable disturbance can likely result in low physiological impact on these animals.     

Cryptosporidium sp. and Giardia sp. infections in mountain gorillas (Gorilla gorilla beringei) of the Bwindi Impenetrable National Park, Uganda

For conservation purposes and because of growing ecotourism, some mountain gorilla (Gorilla gorilla beringei) populations have been habituated to humans. Fecal specimens (n = 100) of nonhabituated and human-habituated gorillas (5 populations; 6 age classes) were tested for Cryptosporidium sp. oocysts and Giardia sp. cysts by conventional staining and immunofluorescent antibody (IFA). Cryptosporidium sp. infections (prevalence 11%) were not restricted to very young gorillas but were observed in 3-yr-old to >12-yr-old gorillas; most of the infections (73%) occurred in human-habituated gorillas. The prevalence of Giardia sp. infections was 2%; 1 nonhabituated gorilla was concomitantly infected. Oocysts of Cryptosporidium sp. in the gorilla stools were morphologically, morphometrically, and immunologically undistinguishable from a bovine isolate of Cryptosporidium parvum oocysts. Mean concentration of Cryptosporidium sp. oocysts and Giardia sp. cysts in gorilla stools was 9.39x10(4)/g, and 2.49x10(4)/g, respectively. There was no apparent relationship between oocyst concentration and gorilla age, sex, or habituation status. Most Cryptosporidium sp. infections found in gorillas with closest proximity to people may be a result of the habituation process and ecotourism. This study constitutes the first report of Cryptosporidium sp. infections in the family Pongidae, in the free-ranging great apes, and in the species of gorilla.     

Systematic relationships of gorillas from Kahuzi Tshiaberimu and Kayonza

Previous classifications of gorillas from Mt. Kahuzi, Mt. Tshiaberimu and the Kayonza Forest, placing them in Gorilla gorilla graueri or G.g. beringei, somewhat over-simplify a complex situation. Both Kahuzi and Tshiaberimu gorillas are close to graueri and should be placed in that subspecies, but each (in different ways) shows some approach to beringei, either through independent adaptation to extreme montane conditions, or because they may be points along a (now disrupted) cline from one race to the other. A hypothesis for the dispersal of beringei is presented, making use of geophysical data on the movement of the African plate over the Virunga 'hot-spot'.     

Pathogen Transmission from Humans to Great Apes is a Growing Threat to Primate Conservation

All six great ape species are listed as endangered or critically endangered by the IUCN and experiencing decreasing population trends. One of the threats to these non-human primates is the transmission of pathogens from humans. We conducted a literature review on occurrences of pathogen transmission from humans to great apes to highlight this often underappreciated issue. In total, we found 33 individual occurrences of probable or confirmed pathogen transmission from humans to great apes: 23 involved both pathogen and disease transmission, 7 pathogen transmission only, 2 positive antibody titers to zoonotic pathogens, and 1 pathogen transmission with probable disease. Great ape populations were categorized into captive, semi-free-living, and free-living conditions. The majority of occurrences involved chimpanzees (Pan troglodytes) (n = 23) or mountain gorillas (Gorilla beringei beringei) (n = 8). These findings have implications for conservation efforts and management of endangered great ape populations. Future efforts should focus on monitoring and addressing zoonotic pathogen and disease transmission between humans, great ape species, and other taxa to ensure the health of humans, wild and domestic animals, and the ecosystems we share.     

Capillaria hepatica (Nematoda) infections in human-habituated mountain gorillas (Gorilla gorilla beringei) of the Parc National de Volcans, Rwanda

Habituation to humans of free-ranging populations of endangered mountain gorillas (Gorilla gorilla beringei) raised concern of anthropozoonotic transmission of parasitic helminths and protozoans. Examinations of liver tissue of 19 gorillas found dead in the Parc National de Volcans, Rwanda, revealed 10 cases of hepatic nematodiasis due to Capillaria hepatica. Identifiable C. hepatica eggs were present in the liver of 4 gorillas (3 juveniles, 1 adult), and nematode cross-sections were found in 1 juvenile gorilla. Six other adult gorillas had areas of periportal and subcapsular fibrosis with calcified eggs. Histologically, the lesions surrounded by the areas of mild inflammatory reaction were characterized by subcapsular, periportal foci of fibrosis in which were embedded numerous C. hepatica eggs. Control of hepatic capillariasis in the remaining populations of mountain gorillas should be focused on eradication or control of populations of rodent pests (i.e., mice and rats) that sustain the reservoir of C. hepatica in habitats shared by gorillas and humans.     

Decaying wood is a sodium source for mountain gorillas

Like several other non-human primates, mountain gorillas (Gorilla beringei beringei) in Bwindi Impenetrable National Park, Uganda consume decaying wood, an interesting but puzzling behaviour. This wood has little obvious nutritional value; it is low in protein and sugar, and high in lignin compared to other foods. We collected pieces of wood eaten and avoided by gorillas, and other foods consumed by gorillas, and measured their sodium content. Wood was substantially higher in sodium than other dietary items, and wood pieces from stumps eaten contained more sodium than those that were avoided. Wood represented only 3.9% of the wet weight food intake of gorillas, but contributed over 95% of dietary sodium, leading us to conclude that decaying wood is an important sodium source for Bwindi gorillas. Because sodium has been leached from the weathered soils characteristic of the subhumid and humid tropics, and because terrestrial plants generally do not require sodium, tropical herbivores, including gorillas, often encounter problems locating the sodium essential for their well-being. Decaying wood is an unexpected sodium source.     

Western lowland gorillas (Gorilla gorilla gorilla) change their activity patterns in response to frugivory

The most important environmental factor explaining interspecies variation in ecology and sociality of the great apes is likely to be variation in resource availability. Relatively little is known about the activity patterns of western lowland gorillas (Gorilla gorilla gorilla), which inhabit a dramatically different environment from the well‐studied mountain gorillas (G. beringei beringei). This study aims to provide a detailed quantification of western lowland gorillas' activity budgets using direct observations on one habituated group in Bai Hokou, Central African Republic. We examined how activity patterns of both sexes are shaped by seasonal frugivory. Activity was recorded with 5‐min instantaneous sampling between December 2004 and December 2005. During the high‐frugivory period the gorillas spent less time feeding and more time traveling than during the low‐frugivory period. The silverback spent less time feeding but more time resting than both females and immatures, which likely results from a combination of social and physiological factors. When compared with mountain gorillas, western lowland gorillas spend more time feeding (67 vs. 55%) and traveling (12 vs. 6.5%), but less time resting (21 vs. 34%) and engaging in social/other activities (0.5 vs. 3.6%). This disparity in activity budgets of western lowland gorillas and mountain gorillas may be explained by the more frugivorous diet and the greater dispersion of food resources experienced by western lowland gorillas. Like other apes, western lowland gorillas change their activity patterns in response to changes in the diet. Am. J. Primatol. 71:91–100, 2009. © 2008 Wiley‐Liss, Inc.     

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

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

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

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

A comparative analysis of temporomandibular joint morphology in the African apes

A number of researchers have suggested a functional relationship between dietary variation and temporomandibular joint (TMJ) morphology, yet few studies have evaluated TMJ form in the African apes. In this study, I compare TMJ morphology in adults and during ontogeny in Gorilla (G.g. beringei, G.g. graueri, and G.g. gorilla) and Pan (P. paniscus, P. troglodytes troglodytes, P.t. schweinfurthii, and P.t. verus). I test two hypotheses: first, compared to all other African apes, G.g. beringei exhibits TMJ morphologies that would be predicted for a primate that consumes a diet comprised primarily of moderately to very tough, leafy vegetation; and second, all gorillas exhibit the same predicted morphologies compared to Pan. Compared to all adult African apes, G.g. beringei has higher rami and condyles positioned further above the occlusal plane of the mandible, relative to jaw length. Thus, mountain gorillas have the potential to generate relatively more muscle force, more evenly distribute occlusal forces along the postcanine teeth, and generate relatively greater jaw adductor moment. G.g. beringei also exhibits relatively wider mandibular condyles, suggesting these folivorous apes are able to resist relatively greater compressive loads along the lateral and/or medial aspect of the condyle. All gorillas likewise exhibit these same shape differences compared to Pan. These morphological responses are the predicted consequences of intensification of folivory and, as such, provide support for functional hypotheses linking these TMJ morphologies to degree of folivory. The African apes to not, however, demonstrate a systematic pattern of divergence in relative condylar area as a function of intensification of folivory. The ontogenetic trajectories for gorillas are significantly elevated above those of Pan, and to a lesser but still significant degree, mountain gorillas similarly deviate from lowland gorillas (G.g. gorilla and G.g. graueri). Thus, adult shape differences in ramal and condylar heights do not result from the simple extrapolation of common growth allometries relative to jaw length. As such, they are suggestive of an adaptive shift towards a tougher, more folivorous diet. However, the allometric patterning for condylar area and condylar width does not systematically conform to predictions based on dietary specialization. Thus, while differences in condylar shapes may confer functional advantages both during growth and as adults, there is no evidence to suggest selection for altered condylar proportions, independent of the effects of changes in jaw size.     

Host-parasite ecology of the helminths in mountain gorillas

To understand patterns of intestinal parasitism in healthy, undisturbed endangered mountain gorillas (Gorilla beringei), we regularly collected fecal samples from a group of 14 wild gorillas residing in Bwindi Impenetrable National Park (BINP), Uganda, for about 1 yr. The objectives of the study were to collect baseline data in order to document the helminth parasites infecting this group of gorillas and to examine the effects of season and host age-sex class on patterns of parasite infection. In addition to weekly surveys of feces from all group members, fecal samples from 4 identified individuals were examined almost daily. We identified the diagnostic stages of the following parasites: strongylids (Strongylida), Anoplocephala gorillae, Probstmayria sp., Strongyloides fuelleborni, and a trematode. Monthly and daily fluctuations in strongylid egg counts were observed. Infants had lower strongylid egg counts compared with other group members. Both of the silverbacks had higher mean egg counts in the wet season than in the dry season. Examination of fecal samples from identifiable gorillas revealed high day-to-day variation in strongylid egg counts. No evidence of anthropozoonotic transmission of intestinal helminths was found.     

Sharing natural resources: mountain gorillas and people in the Parc National des Volcans,Rwanda

The compatibility of natural resource use by people and mountain gorillas (Gorilla beringei beringei) within the Parc National des Volcans was studied. The distribution of gorillas was modelled using a Maximum Entropy algorithm. Biophysical predictor variables were trained with daily GPS locations of gorillas during 2006. Elevation, as a climate surrogate, was the best predictor (58%) of the occurrence of gorillas. The mid‐altitudes (2500–3500 m a.s.l.) contained the bulk of the gorilla groups. Incoming solar radiation, as proxy for comfortable nesting sites, was the second best predictor (17%). Vegetation types, as foliage provider, (13%) and slope steepness for providing security (12%) were contributing predictors. The modelled and actual gorilla distributions were together overlaid with people’s resource use in the park. Both people and gorillas were congregated in the areas identified as most suitable for gorillas. However, within these areas spatial segregation was found between human natural resource‐users and gorillas. Therefore, the number of gorillas is likely to be limited by the human natural resource use within the park. A perimeter fence, the introduction of community‐based natural resource management, and a buffer zone are discussed as short‐, medium‐ and long‐term mitigation measures.     

Diversity of Microsporidia,Cryptosporidium and Giardia in Mountain Gorillas (Gorilla beringei beringei) in Volcanoes National Park,Rwanda

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.     

Conservation successes at micro-, meso- and macroscales

Although large-scale biodiversity declines are ongoing, certain conservation actions have made a positive difference. Rates of extinction and endangerment of vertebrate species, for instance, have probably been reduced via conservation interventions. Such conservation actions operate at different spatial scales. Habitat preservation and endangered species recovery are examples of conservation successes at microscales. Mesoscale conservation includes regional cooperation among neighboring countries that has arrested population declines of endangered species, such as mountain gorillas. At macroscales, public pressure on multinational corporations has sometimes resulted in their abandoning environmentally damaging practices or suppliers with poor environmental records. Overall, conservation projects such as these need more long-term funding and greater political and popular support, and must also include provisions to evaluate and document their outcomes. As we discuss here, a focus on conservation successes achieved at different scales can help to promote these aims and guide future conservation victories.