Effects Of Habitat Overlap On Helminth Transmission Between Sympatric Baboons, Vervet Monkeys And Ungulates In Amboseli Ecosystem, Kenya
In natural ecosystems, helminths and their diverse hosts co-exist as interacting ecological communities, however the factors that determine which helminths (s) infect which host (s) are not well understood. Habitat overlap is predicted to influence helminth transmission and infection patterns, including helminths co-occurrence across sympatric host taxa. The overall objective of this study was to determine the effects of habitat overlap between sympatric hosts on transmission of helminths in Amboseli ecosystem, Kenya. The focal animal was the baboon population, which has been the subject of studies for decades by the Amboseli Baboon Research Project, while the sympatric animals included Vervet monkeys, cattle, sheep, goats (domestic ungulates) and wildebeests, impala, Grant’s gazelles and Thomson’s gazelles (wild ungulates). The Amboseli baboon population is structured in to six social groups, which are well known in terms of their ranges and numbers. The first specific objective of this study was to determine the degree of habitat overlap among the social groups of baboons and between baboons and the other sympatric host species. Key individuals of a baboon social group were tracked daily for 7days and (Global positioning system) GPS coordinates of their point locations uploaded in BIOTAS software to generate home ranges by Minimum Convex Polygons (MCP) method. The home range map, size (km2) and degree of overlap between baboon groups were calculated using the software. The degree of overlap between baboon groups and other sympatric hosts was determined through frequency sightings of the sympatric hosts and their dung pile counts in the home range of each baboon group. Results revealed that the home ranges of each baboon group at 100% MCP overlapped with the ranges of at least four other baboon groups, while home ranges at 50% MCP overlapped with at least one other baboon group home range. Degree of habitat overlap between baboon and sympatric hosts based on mean dung pile counts (94.2) was higher at 100% MCP compared to degree of overlap (25.6) at 50% MCP of baboon habitat. In addition the degree of habitat overlap between baboon and sympatric hosts based on mean frequency sightings was higher (8.8) at 100% MCP compared to degree of overlap (4.5) at 50% MCP of baboon habitat. These results indicated that the degree of overlap across baboon home ranges and between baboon and sympatric hosts varied according to the proportion of habitat used by baboons. The second objective was to determine helminth prevalence, abundance and species richness in all the nine sympatric hosts. Sedimentation and floatation techniques were used to assess 1138 formalin-fixed faecal samples collected in the dry and wet season. A total of 16 types of helminth eggs were identified by both sedimentation and floatation fecal assessment methods. Out of these, eight were nematodes, which included Strongylids, Enterobius sp., Strongyloides spp., Primasubulura sp., Trichuris spp., Streptopharagus sp., unidentified species of Spirurina, and unidentified species of Spirurids. The cestodes included Moniezia expansa and Moniezia benedini. Trematodes included Paramphistomum sp., Fasciola gigantica and Fasciola hepatica. Differences in helminth prevalence were recorded across all host species (χ2 = 200.37, df = 8, p = 0.0001) and between seasons (χ2 = 23.87, df = 1, p = 0.0001), using the sedimentation method. Moreover, prevalence of helminths significantly differed across baboon social groups (χ2 = 22.43, df = 5, p = 0.0001) as well as between seasons with higher prevalence in the dry (χ2 = 13.56, df = 1, p = 0.019) compared to the wet season (χ2 = 18.26, df = 1, p = 0.003). The floatation method also revealed differences in prevalence of helminths across host taxa (χ2 = 54.505, df = 8, p<0.0001). Prevalence of helminths across baboon groups differed significantly (χ2 = 27.754, df = 5, p<0.0001) but not between seasons (χ2 = 1.680, df = 1, p = 0.195). Helminth prevalence obtained by floatation method across all the nine sympatric host species was significantly higher (χ2 = 157.472, df = 1, p<0.001) than when determined by sedimentation method. In contrast, helminth species richness was significantly higher when determined by sedimentation method (χ2 = 132.703, df = 5, p<0.001) than when floatation method was used. Concordance between floatation and sedimentation methods was low (0.101) according to Cohens’ kappa statistic. It was found that mean abundance of helminths varied across host taxa and across baboon social groups. Helminth species richness across the host species community ranged from two to eight, with mean species richness of 5.1 ± 1.9. These results indicate that in a sympatric host community, prevalence, abundance and species richness of helminths was highly variable across host taxa. Similar infection patterns were observed between social groups irrespective of their very close proximity of spatial overlap. Seasonality strongly influenced patterns of helminth infection within and across host species. It is likely that the factors that determine intergroup variation in helminth infection are multiple and includes the demographic structures of social groups such as age and sex and habitat heterogeneities. The third objective was to test the influence of habitat overlap among baboon groups and between baboons and sympatric host species in determining helminth infection patterns. Since the degree of home range overlap between baboon home ranges did not vary at 100% MCP, only values at 50% MCP were tested to determine influence of degree of habitat overlap on helminth prevalence, abundance and species richness. Further, dung pile count and frequency of sighting alternative hosts in baboon home ranges were used as indices of degree of overlap. Specifically, relationships were tested between dung pile counts, mean frequency of animal sightings, Shannon-Wiener diversity index, host species diversity and both helminths prevalence and abundance in baboons. The results indicated a lack of statistical association between degree of habitat overlap across baboon groups and their helminths prevalence, abundance and species richness (p > 0.05). These findings indicate that the degree of habitat overlap between social groups does not influence helminths prevalence, abundance and species richness. Statistical analysis showed that at 50% MCP of baboon home ranges, the degree of overlap (based on dung pile counts) between baboon and sympatric hosts did not significantly influence mean helminth prevalence (r2 = 0.441, t = -1.777, p = 0.150) and mean helminth abundance (r2 = 0.222, t = -1.068, p = 0.3458). Results also indicated that the degree of habitat overlap between baboon and sympatric hosts indicated by ShannonWiener diversity index, host diversity and mean frequency of sightings, did not statistically influence helminth prevalence and abundance. However, host diversity (r2 = 0.665, F(1,4) = 7.594, p = 0.05) and Shannon-Wiener diversity index (r2 = 0.727, F(1,4) = 10.64, p = 0.031) significantly influenced helminths species richness in baboon groups. Both indices showed that the degree of habitat overlap between baboons and other sympatric host species did not significantly influence helminths prevalence and abundance in baboons. However, increased habitat overlap with more diverse communities of sympatric hosts showed a declining trend in helminths species richness in baboons. The fourth objective was to genetically determine the species of nematodes shared among sympatric baboons, vervet monkeys and ungulates in Amboseli ecosystem. A total of 977 DNA samples were extracted from larvae cultured from faecal material collected from all the sympatric hosts during the dry and wet seasons. The DNA was amplified by both mitochondrial and internal transcribed spacers of ribosomal genes followed by sequencing. A total of 67 sequences were used for identification of the nematodes and phylogenetic reconstruction. Strongyloides stercoralis, Strongyloides fuelleborni, Trichostrongylus colubriformis, and Oesophagostomum bifurcum were identified from baboons. Cooperia oncophora was identified from cattle, Haemonchus contortus from goats and Teladosargia circumcincta from Grant’s gazelles. In addition, a nematode that displayed viviparity and identified to be a member of the sub-family Cyathostominae was shared in the six sympatric hosts; baboons, vervet monkeys, Thomson’s gazelle, impalas, goats and cattle. Results indicated that habitat overlap facilitated Cyathostominae sharing across hosts, irrespective of their evolutionary relatedness, which may imply a host shift. Specifically, it was most likely that the viviparous nematode underwent a shift to colonize a new host range that includes unusual hosts for members of the sub-family Cyathostominae. Phylogenetic analysis of Strongyloides fuelleborni demonstrated geographical structuring rather than host structuring; specifically, the species in Kenya were genetically distinct from those previously found in Tanzania, Gabon and Japan. In addition, phylogenetic analysis revealed two genetic populations of S. stercoralis in baboons, which had different evolutionary trajectories. The baboon population harboured helminth species of zoonotic potential (S. fuelleborni, S. stercoralis, O. bifurcum, T. colubrifomis), which is a risk to the pastoral community in Amboseli ecosystem. Overall, the results from this study demonstrate that habitat range of baboon social groups exhibited variable overlap with other baboon groups, however overlap did not influence helminth infection patterns across social groups. Further, the overlap between baboons and other sympatric hosts was variable, but the degree of overlap did not significantly influence helminth prevalence and abundance, except helminths species richness across baboon groups. This study also found out that in sympatry, multiple species of helminths, Cyathostominae, Trichuris spp., Moniezia benedini, Moniezia expansa, Primasubulura sp., Enterobius sp., and Spirurina, were commonly shared but at different levels across host taxa, with some hosts harboring more helminths richness than others. Specifically, baboon harboured more helminths species than any host in the community. This is the first study in Kenya to determine helminth infection pattern in a multi-host community involving both wildlife and livestock that belong to multiple phylogenies. Presence of Oesophagostomum bifurcum, Enterobius sp., Strongyloides sp., Trichostrongylus colubriformis in the Amboseli animal community is of public health interest because of their zoonotic potential, hence this study recommends a study to determine their prevalence in the human community in the region.