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

Joseph Wang’Ang’A Oundo,Maamun Jeneby,Daniel Obado Ouso,Lillian Wambua,Ali Abdulahi Musa,George Ong’Amo,Edward Edmond Makhulu,Moses Yongo Otiende,Jandouwe Villinger,Sam R Telford Iii

doi:10.1371/journal.pone.0228366

Abstract

The role of questing ticks in the epidemiology of tick-borne diseases in Kenya’s Maasai Mara National Reserve (MMNR), an ecosystem with intensified human-wildlife-livestock interactions, remains poorly understood. We surveyed the diversity of questing ticks, their blood-meal hosts, and tick-borne pathogens to understand potential effects on human and livestock health. By flagging and hand-picking from vegetation in 25 localities, we collected 1,465 host-seeking ticks, mostly Rhipicephalus and Amblyomma species identified by morphology and molecular analysis. We used PCR with high-resolution melting (HRM) analysis and sequencing to identify Anaplasma, Babesia, Coxiella, Ehrlichia, Rickettsia, and Theileria pathogens and blood-meal remnants in 231 tick pools. We detected blood-meals from humans, wildebeest, and African buffalo in Rh. appendiculatus, goat in Rh. evertsi, sheep in Am. gemma, and cattle in Am. variegatum. Rickettsia africae was detected in Am. gemma (MIR = 3.10) that had fed on sheep and in Am. variegatum (MIR = 250) that had fed on cattle. We found Rickettsia spp. in Am. gemma (MIR = 9.29) and Rh. evertsi (MIR = 200), Anaplasma ovis in Rh. appendiculatus (MIR = 0.89) and Rh. evertsi (MIR = 200), Anaplasma bovis in Rh. appendiculatus (MIR = 0.89), and Theileria parva in Rh. appendiculatus (MIR = 24). No Babesia, Ehrlichia, or Coxiella pathogens were detected. Unexpectedly, species-specific Coxiella sp. endosymbionts were detected in all tick genera (174/231 pools), which may affect tick physiology and vector competence. These findings show that ticks from the MMNR are infected with zoonotic R. africae and unclassified Rickettsia spp., demonstrating risk of African tick-bite fever and other spotted-fever group rickettsioses to locals and visitors. The protozoan pathogens identified may also pose risk to livestock production. The diverse vertebrate blood-meals of questing ticks in this ecosystem including humans, wildlife, and domestic animals, may amplify transmission of tick-borne zoonoses and livestock diseases.

Highlights

Wildlife ecosystems are known to be hotspots for a range of emerging diseases threatening human and livestock health [1,2,3]
This study provides molecular evidence of the presence of the zoonotic R. africae, uncharacterized Rickettsia spp. and veterinary pathogens in questing ticks collected from the Maasai Mara National Reserve (MMNR)
This study provides insights into the diversity of ticks, their microbes, and their blood-meal sources in the Maasai Mara ecosystem in Kenya, which is marked by rapid changes in land-use and considerable encroachment by humans and livestock

Summary

Introduction

Wildlife ecosystems are known to be hotspots for a range of emerging diseases threatening human and livestock health [1,2,3]. Significant land fragmentation has occurred in the Maasai Mara to accommodate an increasing number of conservancies, tourist lodges, human settlements, and agricultural developments [14]. Multiple land uses, such as pastoralism, commercial ranching, camping, tourism, and illegal grazing are being practiced concurrently, which favor the convergence of humans and domestic animals with wild animals and increase the risk of pathogen transmission [14,15,16,17]. We based our study on questing ticks because this is the active stage of ixodid ticks seeking vertebrate hosts for blood-meals in which they pick up new pathogens and transmit them from previous blood-meals to new hosts, including humans and livestock

Methods

Results

Discussion

Conclusion