Survey of ticks and tick-borne pathogens in wild chimpanzee habitat in Western Uganda

Abstract

Background Ticks and tick-borne pathogens significantly impact both human and animal health and therefore are of major concern to the scientific community. Knowledge of tick-borne pathogens is crucial for prescription of mitigation measures. In Africa, much research on ticks has focused on domestic animals. Little is known about ticks and their pathogens in wild habitats and wild animals like the endangered chimpanzee, our closest relative. Methods In this study, we collected ticks in the forested habitat of a community of 100 chimpanzees living in Kibale National Park, Western Uganda, and assessed how their presence and abundance are influenced by environmental factors. We used non-invasive methods of flagging the vegetation and visual search of ticks both on human team members and in chimpanzee nests. We identified adult and nymph ticks through morphological features. Molecular techniques were used to detect and identify tick-borne piroplasmids and bacterial pathogens. Results A total of 470 ticks were collected, which led to the identification of seven tick species: Haemaphysalis parmata (68.77%), Amblyomma tholloni (20.70%), Ixodes rasus sensu lato (7.37%), Rhipicephalus dux (1.40%), Haemaphysalis punctaleachi (0.70%), Ixodes muniensis (0.70%) and Amblyomma paulopunctatum (0.35%). The presence of ticks, irrespective of species, was influenced by temperature and type of vegetation but not by relative humidity. Molecular detection revealed the presence of at least six genera of tick-borne pathogens (Babesia, Theileria, Borrelia, Cryptoplasma, Ehrlichia and Rickettsia). The Afrotopical tick Amblyomma tholloni found in one chimpanzee nest was infected by Rickettsia sp. Conclusions In conclusion, this study presented ticks and tick-borne pathogens in a Ugandan wildlife habitat whose potential effects on animal health remain to be elucidated. Graphical Abstract

Diversity and phylogeny of the tick-borne bacterial genus Candidatus Allocryptoplasma (Anaplasmataceae)

“…Combining our present study with the current literature sequences indicates that there is molecular evidence of Ca. Allocryptoplasma DNA in at least nine tick species in Europe, Asia, Africa, and North and South America, and also in mice and lizards in Europe [ 4 , 14 , 20 , 22 , 27 – 29 , 32 , 34 , 37 , 40 ]. Phylogenetic and genetic analyses further confirm that these Ca.…”

“…In South America, A. coelebs is specialized on mammals [ 5 ] and can readily bite humans [ 39 ], but A. dissimile feed exclusively on reptiles and amphibians [ 5 ]. In Africa, H. parmata is a global generalist, while A. tholloni tends to feed on elephants, but both can bite Hominidae, at least occasionally [ 22 ]. Humans are therefore exposed to bites of Ca.…”

“…Diverse strains of Ca. Allocryptoplasma were also detected in Haemaphysalis parmata and Amblyomma tholloni ticks collected in a wild chimpanzee habitat in Uganda [ 22 ], Amblyomma dissimile in Brazil [ 28 ] and in harvest mites of lizards, Neotrombicula autumnalis , in Italy [ 27 ]. While these bacteria have never been isolated, DNA of similar Ca.…”

“…Allocryptoplasma sp. and Anaplasma -like bacteria [ 4 , 20 , 22 , 27 – 29 , 32 , 37 , 40 ]. However, the use of 16S rRNA gene sequences as an exclusive taxonomic marker was recently shown to be inadequate for inferring a reliable phylogeny within the Anaplasmataceae since the tree topology is often poorly resolved and usually unstable because of insufficient sequence polymorphism [ 7 ].…”

Detection of Anaplasma and Ehrlichia bacteria in humans, wildlife, and ticks in the Amazon rainforest

“…All Ehrlichia , Anaplasma , and Ca . Allocryptoplasma positive samples were further confirmed through independent PCR amplifications using 16S rDNA species-specific primers and, for a subsample of positive samples, using gltA species-specific PCR assays (Supplementary Table 5 ) 53 . PCR products were visualized through electrophoresis in a 1.5% agarose gel.…”