Date Published: June 10, 2019
Publisher: Public Library of Science
Author(s): Vincent Obanda, Ndichu Maingi, Gerald Muchemi, Chege J. Ng’ang’a, Samer Angelone, Elizabeth A. Archie, Emmanuel Serrano.
Gastrointestinal parasites are neglected infections, yet they cause significant burden to animal and human health globally. To date, most studies of gastrointestinal parasites focus on host-parasite systems that involve either a single parasite or a host species. However, when hosts share habitat and resources, they may also cross-transmit generalist gastrointestinal parasites. Here we explore multi-host-parasite interactions in a single ecosystem to understand the infection patterns, especially those linked to livestock-wildlife interfaces and zoonotic risk.
We used both coprological methods (flotation and sedimentation; N = 1,138 fecal samples) and molecular identification techniques (rDNA and mtDNA; N = 18 larvae) to identify gastrointestinal parasites in nine sympatric host species (cattle, sheep, goats, wildebeest, Grant’s gazelles, Thomson’s gazelles, impala, vervet monkeys and baboons) in the Amboseli ecosystem, Kenya.
We found that the host community harbored a diverse community of gastrointestinal helminths, including 22 species and/or morphotypes that were heterogeneously distributed across the hosts. Six zoonotic gastrointestinal helminths were identified: Trichuris spp., Trichostrongylus colubriformis, Enterobius spp. Oesophagostomum bifurcum, Strongyloides stercoralis and Strongyloides fuelleborni. The dominant parasite was Trichuris spp, whose ova occurred in two morphological types. Baboons were co-infected with Strongyloides fuelleborni and S. stercoralis.
We found that the interface zone shared by wild ungulates, livestock and non-human primates is rich in diversity of gastrointestinal helminths, of which some are extensively shared across the host species. Closely related host species were most likely to be infected by the same parasite species. Several parasites showed genetic sub-structuring according to either geography or host species. Of significance and contrary to expectation, we found that livestock had a higher parasite richness than wild bovids, which is a health risk for both conservation and livestock production. The zoonotic parasites are of public health risk, especially to pastoralist communities living in areas contiguous to wildlife areas. These results expand information on the epidemiology of these parasites and highlights potential zoonotic risk in East African savanna habitats.
Increased rates of incursion by people and livestock into wildlife areas, and the consequential interaction and exposure in the shared habitat, can have significant epidemiological consequences, especially for emerging infectious diseases, cross-transmission, and pathogen evolution [1–3]. Understanding parasite dynamics at such interfaces is therefore important to human and animal health, species conservation, and to designing effective prevention and control strategies against parasites [4–7]. In addition, human pastoralist communities share many environmental resources with domestic and wild animals, are at high risk of infection with zoonotic gastrointestinal parasites .
We identified a rich diversity of nematodes, trematodes and cestodes by egg morphology (Table 1) and molecular techniques. The total number of parasite taxa identified by both techniques was 22 (Table 2). Nematodes included Enterobius spp. (Fig 1A), Strongyloides spp. (Fig 1B), strongylid ova (Fig 1C), Primasubulura spp. (Fig 1D), Trichuris spp. (Figs 2A and 2D), Spirurina spp. (Fig 3A), Streptopharagus spp. (Fig 3B) and unidentified Spirurids (Fig 3C and 3D). The identified trematodes were Paramphistomum spp. (Fig 3E) and Fasciola spp. (Fig 3F). The cestodes were Moniezia expansa (Fig 2B) and M. benedini (Fig 2C). Within Moniezia spp. and Trichuris spp., we noted multiple egg morphotypes, which we categorized into operational taxonomic units (OTUs)—a proxy for grouping similar organisms, here specifically used to group nematode eggs with similar dimensions. These included M. benedini OTU A (92.2 by 79.2 μm) whose mean egg dimensions were larger compared to OTU B (61.6 by 58.4 μm), and Trichuris OTU C (73.5 by 36.1 μm) whose mean egg dimensions were larger than OTU D (60.1 by 29.9 μm). Based on morphological parasite identities, host species harbored significantly more helminth parasite taxa (t = 3.577, df = 8, p = 0.0072) in the wet season as compared to the dry season (Table 1). With the additional information provided by genetic markers, we found a total of 22 distinct parasite taxa (Table 2), with the highest parasite richness observed in non-human primates, followed by livestock and least in wild ungulates. Baboons exhibited the highest parasite richness; however, this difference was likely because of our greater sampling effort in baboons samples (we searched 185 baboon samples per season as compared to 48 samples for the other host species).
This is the first study to assess parasite diversity in a sympatric host community that includes bovids (livestock and wild ungulates) and non-human primates. Our results reveal a dynamic parasite-host interaction characterized by parasite sharing among hosts, yet restricted by host evolutionary history. The combination of coprological and molecular tools has facilitated the detection of a rich diversity of parasites, including the differentiation of nematode species whose eggs are morphologically indistinguishable and often included in the generic category of ‘strongyle eggs’, which does not allow the exact parasite richness of the host to be known. The taxonomic diversity detected in the ungulates and primates from Amboseli includes species that are of veterinary and public health importance and whose epidemiology and phylogeography is less known in Kenya. In addition, we found that seasonality was linked to parasite richness such that hosts had higher diversity in the wet compared to dry season (Table 1). This pattern agrees with current scientific understanding of seasonal effects on helminth propagation, environmental persistence and transmission [37–39].
It is clear that in a multi-species animal community like in the Amboseli ecosystem, parasite interaction with their hosts is so dynamic but also structured. For instance, some parasites infect multiple species across host taxa, while some tend to be restricted within hosts that are closely related. Clearly, bovids did not share gastrointestinal helminths with the non-human primates and even though Trichuris spp. was present in all the hosts, the morphotypes in bovids differed from those in non-human primates. In addition, we observed that each host had variable diversity of parasites, and unexpectedly, livestock had more diversity compared to wild ruminants. The bidirectional exchange of these parasites between wild ungulates and livestock is thus plausible and has potential implications on conservation and livestock productivity as well as anti-helminth control in this region. Most of the species found in non-human primates, Trichuris spp., T. colubriformis, Enterobiusspp., O. bifurcum, S. stercoralis and S. fuelleborni are zoonotic and represent a potential risk to the pastoralist communities.