Pathogens, endosymbionts, and blood-meal sources of host-seeking ticks in the fast-changing Maasai Mara wildlife ecosystem

Abstract

BackgroundThe role of questing ticks in the epidemiology of tick-borne diseases in Kenyas Maasai Mara National Reserve (MMNR), an ecosystem with intensified human-wildlife-livestock interactions, remains poorly understood. Therefore, we carried out a survey of the diversity of questing ticks, their blood-meal hosts, and tick-borne pathogens to understand potential effects to human and livestock health. MethodsQuesting ticks were collected by flagging and hand picks from vegetation in 25 localities and identified based on morphologic and molecular criteria. We used PCR with high-resolution melting (HRM) analysis, and sequencing to identify Anaplasma, Babesia, Coxiella, Ehrlichia, Rickettsia, and Theileria pathogen diversities and blood meals in 231 tick pools. ResultsA total of 1,465 host-seeking ticks were collected, including Rhipicephalus appendiculatus (n = 1,125), Rhipicephalus pulchellus (n = 6), Rhipicephalus evertsi (n = 5), Amblyomma cf. gemma (n = 178), Amblyomma gemma (n = 145), Amblyomma variegatum (n = 4), Amblyomma sp. (n = 1), and Haemaphysalis leachi (n = 1). Remnant blood-meals from humans, wildebeest, and African buffalo were detected in Rh. appendiculatus, goat in Rh. evertsi, sheep in Am. gemma, and cattle in Am. variegatum. Rickettsia africae was detected in Am. gemma (1/25 pools) that had blood-meal remnant from sheep and Am. variegatum (4/25 pools) that had fed on cattle. Rickettsia spp. were found in Am. gemma (4/25 pools) and Rh. evertsi (1/4 pools). Anaplasma ovis was detected in Rh. appendiculatus (1/172 pools) and Rh. evertsi (1/4 pools), while Anaplasma bovis was detected in Rh. appendiculatus (1/172 pools). Theileria parva was detected in Rh. appendiculatus (27/172 pools). Babesia, Ehrlichia and Coxiella pathogens were not found in any ticks. Unexpectedly, diverse Coxiella sp. endosymbionts were detected in all tick genera (174/231 pools). ConclusionsThe data shows that ticks from the rapidly-changing MMNR are infected with zoonotic R.africae and unclassified Rickettsia spp, demonstrating the persistent risk of African tick-bite fever and other and Spotted Fever Group rickettsioses to local dwellers and visitors to the Maasai Mara ecosystem. Protozoan pathogens that may pose risk to livestock production were also identified. We also highlight possible existence of morphotypic variants of Amblyomma species, based on the observation of Ambyomma cf. gemma, which may be potential human parasites or emergent disease vectors. Our findings also demonstrate that questing ticks in this ecosystem have dynamic vertebrate blood sources including humans, wildlife and domestic animals, which may amplify transmission of tickborne zoonoses and livestock diseases. Further studies are needed to determine the role of Coxiella endosymbionts in tick physiology and vector competence.