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

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-bor...

Full description

Bibliographic Details
Main Authors: Joseph Wang'ang'a Oundo, Jandouwe Villinger, Maamun Jeneby, George Ong'amo, Moses Yongo Otiende, Edward Edmond Makhulu, Ali Abdulahi Musa, Daniel Obado Ouso, Lillian Wambua
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2020-01-01
Series:PLoS ONE
Online Access:https://doi.org/10.1371/journal.pone.0228366
id doaj-06de4fa7466343388d7d53de99b3892c
record_format Article
spelling doaj-06de4fa7466343388d7d53de99b3892c2021-03-03T21:58:15ZengPublic Library of Science (PLoS)PLoS ONE1932-62032020-01-01158e022836610.1371/journal.pone.0228366Pathogens, endosymbionts, and blood-meal sources of host-seeking ticks in the fast-changing Maasai Mara wildlife ecosystem.Joseph Wang'ang'a OundoJandouwe VillingerMaamun JenebyGeorge Ong'amoMoses Yongo OtiendeEdward Edmond MakhuluAli Abdulahi MusaDaniel Obado OusoLillian WambuaThe 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.https://doi.org/10.1371/journal.pone.0228366
collection DOAJ
language English
format Article
sources DOAJ
author Joseph Wang'ang'a Oundo
Jandouwe Villinger
Maamun Jeneby
George Ong'amo
Moses Yongo Otiende
Edward Edmond Makhulu
Ali Abdulahi Musa
Daniel Obado Ouso
Lillian Wambua
spellingShingle Joseph Wang'ang'a Oundo
Jandouwe Villinger
Maamun Jeneby
George Ong'amo
Moses Yongo Otiende
Edward Edmond Makhulu
Ali Abdulahi Musa
Daniel Obado Ouso
Lillian Wambua
Pathogens, endosymbionts, and blood-meal sources of host-seeking ticks in the fast-changing Maasai Mara wildlife ecosystem.
PLoS ONE
author_facet Joseph Wang'ang'a Oundo
Jandouwe Villinger
Maamun Jeneby
George Ong'amo
Moses Yongo Otiende
Edward Edmond Makhulu
Ali Abdulahi Musa
Daniel Obado Ouso
Lillian Wambua
author_sort Joseph Wang'ang'a Oundo
title Pathogens, endosymbionts, and blood-meal sources of host-seeking ticks in the fast-changing Maasai Mara wildlife ecosystem.
title_short Pathogens, endosymbionts, and blood-meal sources of host-seeking ticks in the fast-changing Maasai Mara wildlife ecosystem.
title_full Pathogens, endosymbionts, and blood-meal sources of host-seeking ticks in the fast-changing Maasai Mara wildlife ecosystem.
title_fullStr Pathogens, endosymbionts, and blood-meal sources of host-seeking ticks in the fast-changing Maasai Mara wildlife ecosystem.
title_full_unstemmed Pathogens, endosymbionts, and blood-meal sources of host-seeking ticks in the fast-changing Maasai Mara wildlife ecosystem.
title_sort pathogens, endosymbionts, and blood-meal sources of host-seeking ticks in the fast-changing maasai mara wildlife ecosystem.
publisher Public Library of Science (PLoS)
series PLoS ONE
issn 1932-6203
publishDate 2020-01-01
description 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.
url https://doi.org/10.1371/journal.pone.0228366
work_keys_str_mv AT josephwangangaoundo pathogensendosymbiontsandbloodmealsourcesofhostseekingticksinthefastchangingmaasaimarawildlifeecosystem
AT jandouwevillinger pathogensendosymbiontsandbloodmealsourcesofhostseekingticksinthefastchangingmaasaimarawildlifeecosystem
AT maamunjeneby pathogensendosymbiontsandbloodmealsourcesofhostseekingticksinthefastchangingmaasaimarawildlifeecosystem
AT georgeongamo pathogensendosymbiontsandbloodmealsourcesofhostseekingticksinthefastchangingmaasaimarawildlifeecosystem
AT mosesyongootiende pathogensendosymbiontsandbloodmealsourcesofhostseekingticksinthefastchangingmaasaimarawildlifeecosystem
AT edwardedmondmakhulu pathogensendosymbiontsandbloodmealsourcesofhostseekingticksinthefastchangingmaasaimarawildlifeecosystem
AT aliabdulahimusa pathogensendosymbiontsandbloodmealsourcesofhostseekingticksinthefastchangingmaasaimarawildlifeecosystem
AT danielobadoouso pathogensendosymbiontsandbloodmealsourcesofhostseekingticksinthefastchangingmaasaimarawildlifeecosystem
AT lillianwambua pathogensendosymbiontsandbloodmealsourcesofhostseekingticksinthefastchangingmaasaimarawildlifeecosystem
_version_ 1714814020900356096