Heterogeneity in patterns of helminth infections across populations of mountain gorillas (Gorilla beringei beringei)

Abstract

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.

Figure 1

Division of the Virunga Massif into four areas according to volcano positions (M: Mikeno, Virunga National Park; K_V: Karisimbi–Visoke, Volcanoes National Park; V_S: Visoke–Sabyinyo, Volcanoes National Park; S_M: Sabyinyo–Muhavura, Mgahinga Gorilla National Park, Volcanoes National Park) with vegetation zones (based on Robbins et al.) and distribution of the studied groups. Map was created using ArcGIS Desktop 10.6 (ESRI 2019. ArcGIS Desktop: Release 10.6. Redlands, CA: Environmental Systems Research Institute; esri.com). Vegetation data were adopted according to Robbins et al.; boundaries of protected areas were derived from ProtectedPlanet.net database.

Figure 2

Examined host and their parasites quantified in the study: (A) resting group of mountain gorillas in Virunga Massif (Virunga National Park, Democratic Republic of the Congo); (B) egg of strongylid nematode; (C) egg of anoplocephalid tapeworm; both microphotographs in the same scale.

Figure 3

Models’ predicted mean values with 95% confidence intervals for the factors affecting helminth infections in mountain gorillas in Virunga Massif and Bwindi Impenetrable National Park (dataset 1). (A) strongylid eggs per gram (EPG)—sampling area and age/sex class effects, (B) tapeworm EPG—sampling area and group size effects, (C) tapeworm EPG—sampling area and age/sex class effects. juv/sub: juvenile/subadult class; M: Mikeno (Virunga National Park); K_V: Karisimbi–Visoke (Volcanoes National Park), V_S: Visoke–Sabyinyo (Volcanoes National Park), S_M: Sabyinyo–Muhavura (Mgahinga Gorilla National Park, Volcanoes National Park).

Figure 4

Models’ predicted mean values with 95% confidence intervals for the factors affecting helminth infections in mountain gorillas in Virunga Massif in two periods (dataset 2). (A) strongylid egg per gram (EPG)—sampling area and group size effects, (B) strongylid EPG—sampling area and age/sex class effects, (C) tapeworm EPG—sampling area and group size effects, (D) tapeworm EPG—sampling area and age/sex class effects. juv/sub: juvenile/subadult class; M: Mikeno (Virunga National Park); K_V: Karisimbi–Visoke (Volcanoes National Park), V_S: Visoke–Sabyiniyo (Volcanoes National Park), S_M: Sabyinyo–Muhavura (Volcanoes National Park).

Figure 5

Models’ predicted mean values with 95% confidence intervals for the factors affecting helminth infections in individually sampled mountain gorillas in Virunga Massif (dataset 3). (A) strongylid eggs per gram (EPG)—group identity and age effects, (B) strongylid EPG—sampling period (season) and group identity effects, (C) tapeworm EPG—group identity and age effects, (D) tapeworm EPG—sampling period (season) and group identity effects.